A Review by CU2 micro-organisms - DBK Groupdbkgroup.org/Papers/dixon_inhib_jab89.pdf · 6. Preserva!ion ol meat and fish by COI, f 14 6.1. Inhibition ol the growth and metabolism

Journal 01 Apptied Bacteriology 1989,67, 109-136

A Review

The inhibition by CU2 of the growth and metabolism of micro-organisms

NEIL M. DIXON & DOUGLAS B. KECL* Deportment ofBioiogical Sciertces, University College of tYnles, Aberystwyth, Dyf'ed, SY23 3 D A , UK

Raceioed 17 August f 988

1. Introduction, 109 2 'CO; concentralions, 110

2.1. Dissolved CO, concentralion, 1 10 - 2.2. Bicarbonate concentration in a pH-controlled culture with a constant

temperature and gas phase, 11 0 3. Historical, 1 I I 4. Treatmen! o l water with CO, , I I I 5. Tratmcnl 01 dairy products with GO,, 1 I3 6. Preserva!ion ol meat and fish by COI, f 14

6.1. Inhibition o l the growth and metabolism of rood-spoilage micro-organisms, 1 14 6.2. CO,-resistance OF rood-related bacteria, 1 16 6.3. CO, in the prcvcnzion of rood spoilage by clostridia. 1 16 6.4. Pr~blems associalcd with the preservation of mea t by CO1-containing

atmospheres, 1 16 6 5 . Prestrvalion oT seafood by CO,-containing atmospheres, 117

7. Preservation or fruit and vegiables by CO,, 118 8. Control aT the praduerion or fermented foods and beverages using CO, . 119 9. Inhibition or other industrial fermentation processts by CO,. 119

9.1. Effects a i CO, an the production of biomass, 1 19 9.2. Effects of CO, on the production of biochemicals. 121 9.3. EKects or CO, on the Ircatrncnl or wastes, 12 I

10. S i t s or action, 122 10.1. Biological membranes, 122

10.1.1. The metabolic control analysis, 123 10.2 Cytoplasmic enzymes as a site of action, af CO 124

10.21. CO,-controlled induclion/rcpression aT enzyme synthesis, 124 10.2.2. CO,-inhibition or enzyme reactions, 124

I I . Mechanisms of CO, inhibition or microbial growth and rnetaboIism, 125 12. Concluding remarks, 127 13. Acknowlcdgerntnls. 127 14. References, I28

I t has been known for many years that the growth and metabolism of micro-organisms is accornpan- ied by the uptake and/or evolution of mrbon dioxide. Yet, except for the obvious case or autotrophic micro-organisms, the partial pressure of CO, bC02) has rarely been considered to be of much quantitative significance to the physiology 01 r he e l l . Although there hare k e n a number of reviews on the cfftcts or CO, on the requirement For and fixation o l CO, by microorganisms, especially autotrophic ones (e.g. Fuchs & Stuppcrich 1983; Codd 1984; Fuchs 19861, in general little attention appears ro have been concentrated on what are in Fact a rather widespread sct af studies concerning

* Corresponding author.

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COI inhibition. Nonetheless, CO, is inhibitory to the growth of a number of micro-organisms, a fact which has enjoyed increasing exploitat ion in the preservation or foods1 uffs from bacterial spoilage, It thercfotc sccrned appropriate to collate and summarize this material, a survey which forms the subjecl matter of the prescnt review. Aher an historical introduction, the use of 60, as an antimicrobial agent for use in the preparation of potables and consumablcs is considered. This leads naturally to a review of some 01 the antimicrobial properties OF C03 during industrial fermentations. Many or these observations have been of a somewhat empirical nature; thus, finally we consider some or the more molecular or mechanistic studies which have sought to ascertain the means by which CO, might be acting to cause microbial growth inhibition. We begin with a brier discussion of the therrno. dynamics of the interactions of CO, and aqueous media.

Although the partial pressure oiCO, in the gas phase may be held constant, the ratios of the different possible species of 'CO,' in the aqueous phase will vary as a function of the pH and other factors. Since CO, can hydrate and dissociate in water, the reaction scheme may be written as (Knoche 1980):

In addition it has recently been proposed that small concentrations of dimeric hydrogen carbonate ions (H,C,Oi) exist near neutral pH (Covington 1985). Since thc concentcatian or this specics is negligible, however, such ions will not be considered in the folEowing. At pH values less than 8, the concentration of carbonate ions may be neglected (Yagi & Yoshida 1977) and only the following hydration reactions need to be considered:

2.1. DISSOLVED COz CONCENtRhTlON

The canccntration of C 0 2 in solution (CCO,]aq) is normally expressed by Henry's law (Butler 1982; H o et of. 1987):

where K, = the Henry's law constant (in units ot rnolfl atm) and pCOi = ihe partial pressure ofC02 in the gas phase (in atm). For cultures grown under atmospheric pressure, the proportionality of solubility and partial pressures (Henryes law) may be assumcd without iniroducing appreciable errors {Schumpe et al. E 982).

At a temperacure or 37"C, K, = 10-''61 (Butler 1982) where the LCO,] is expressed in molar terms. Thus to obtain [COJ in rnillimolar terms, K H = 101'39. Hence:

In oLher words, when pCO, = 1 atrn, the concentration or dissolved CO, = 24-6 rnrnoffl.

2.2. BtCARBONATE CONCENTRkTlON IN a pH-CONTROLLED CULTURE W l f H A CONSTANT TEXIPERATURE A N D G A S PHASE

The equilibrium bemeen CO, and HCO, is defined by a 'hybrid' equilibrium constant K', (Butlcr 1982) where

From eqn (4) i t follows that:

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CO, inhibit ioft 111

pk; is to the thermodynamic pK of the reaction p ~ f and the ionic strength 1 by:

From Davits's equalion {ButIer t 9821,

here T is the zcmperature in "C. 1 is the ionic strength or the medium and i s given by

1 = 112 xc,z: (8)

where ci = the conccnt ration of ion i and z, = the charge on ion i. TO obtain the apparent pK,, , Tor the CO,/HCO; equilibrium, wc use (Ruller 1982)

heref fore from eqn (9) we obtain pK, , , and so from cqn ( 5 )

A typical value of pK,, , is 6-3 (at zero ionic strength and 35'C Butler 1982). Thus the addition of CO, to an aqueous medium will tend to cause the pH to drop to a-value approximately equal lo the pK, depending upon the other burrering constituents in the medium.

Carbon dioxide was known to the ancients. Its presence was pertseived by PEenius near volcanoes and mineral springs and i t was called by him 'spiritus letales'(Valtey & Rettger 1927). 1 ohn Baptista van Helrnonl, introducing the word gas, callcd it 'gas sylvestre' (Valley & Rettger 1927). He knew that this gas could extinguish a flame and cause sumocation in animals. It is possible that these, now well- known, properlics mused thc efforts or the earlier workers to bc for thr: most part directed towards a study of the inhibitory aclion OF CO, an the growth bt bacteria. Amongst the earliest work concerning the influence of CO, on bacteria was that of Pasteur & Joubect (1 8771, who reported that Bacillsrs anthracis was killed by CO1. No mention was made, however, of the media used, the length of the exposure to CO,, or the concentration of CO, required for a fatal cCTect. Further research showed that exposure to an almost pure atmosphere of CO, for 5-8 h did not in fact kill B. anthracis, nor even alter its pathogenicity (Szpilman 1880), although rcsults from around this time were often con- tradictory (e.g. d'drsonval & Charrin 1893; Sabrazes & Barin 1893). Barferitrm ryphosum (Salmonella typhi) and B. anrhracis upere found by Schaffer & Freudenreich (1891) to be unaffected in broth cultures under 7 atrn pressure of CO, . (N.B. 1 atm pressure = 14.696 IbffinZ = 101 325 Pa = 760 mrn Ilg; despite the [act that alm are not SI units, the widespread usage of this unit, and the intuitive reel for what i t represents, Ieads to the retenlion of ils usage herein.) J t was also reported that CO, does not kill bacteria, but inhibits motility, whercas small amounts orCOz stirnulaled motility (Grossman & Mayerhausen 18771, In contrast to this, CO, was found to be toxic to h3enEngococcus spp. and to exert a rapid toxic effect upon Spirochaeta pallida (Shaw-Mackenzie 1918). I t was mentioned in the same paper that CO, gas could bc uscd bcncficially in the treatrncnt or open wounds and ulcerations, as well as by rectal infroduction in cases of dysentery! That the inhibitory effect of CO, is organism- dependent appears first to have been shown by Buchner ( 1 885), in that CO, inhibited Koch's Vibrio, but growth was obtained with Ficth's Aethy!bacjllus, the Napel choIera baciIlus and Salm. typhi.

4. Treatment ofwater with CO,

About the turn of the century, carbonation was being investigated as a trealrnent for the improve- ment of the quality of water, milk and milk products. Jn fact, the carbonation of beverages is today one of the largest appIications of CO, (Reichert f 982). Redudion in bacterial numbers in Munich city water was obraincd in thc laboratory by carbonating thc water at atmospheric pressure, but stcriliza- tien was not reported (Leone 1886). That it was CO,, and nor the lack aT oxygen, that caused the decrease in bacterial nvrnbcrs had been demonstrated earlier (Leone 1885). Artikally carbonated

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TaMc t. The effect of pH and CO, on the growth of micro-organisms (Ha)% 01.1959)

Carbon dioxide Nit ropen

Controls Samplm Controls Samples - Organism PH Growth pH Growth pH Growth Growth

- -- -

K lehsielb amogenrs 6- 7 + + 5.6 - 5-6 ++ ++ Clostridium botulinum 6.9 -k -t 5-4 f 5.4 ++ + Clnsrridium buryricum 5.5 4- + 5-0 1 5.0 - t i + + C l ~ ~ ~ r i d i u m sporogenes 6.9 4- + 5-4 - + 5 -4 ++ + + St apl~ylocaccus arrreus 6.7 ++ 5-6 A 5.6 ++ ++ Saccl~oromyces cerecisiae 5.5 + + 5.0 - 5.0 -I-+ ++ Pink lcrula 5-5 + + 5.0 - 5.0 ++ + + Aspergillus ntger 5-5 + + + 5.0 5 5-0 f + + ++

Conlrols were not gassed whereas the sarnplcs were pressurized to approxima~eIy 6 atm of either CO, or N, . nlc pH or the CO, controls war; the "normal' pH ai the medium, the pH of the CO, samples was thc pH attcr the addition of the CO, and the pH for the N, controls and samples was adjusted lo match nbai for I he 60, snmpls. The degree or growlh was defined as Collows: -F f + , luxuriant mould grawt h with aerial hyphae; f +, marked incrcasc in colony count over initial count or moderate rndutd grow111; +, definite growth or slight to modetale increasc in colony count; +, colony count remained apptox- imatcly equal to the iniiial count; -, slight decrease in colony count frorn_lhe initial count or no evidence of mould growth.

waters, distilled water and Berlin city walcr were used to demonstrate that carbonation removed the danger from cholera, but that thcrc was still danger lrom typhoid fever, since Salrn. typhi remained viable in carbonated waters for from 5 to 7 d (Hochstetter 1887), and in somc cases growth continued unhindered [Friinkef 1889; Frankland 1896). Vibrl'o cholerae, R. antfiracis, Slaplr~lococctts ntrrerrs, Staph. albus, Snlm. rypl~i and 'B. llepisepficum' wc,m not nffcctcd by the concentration of CO, naturally dissolved (from the atmosphere) in water at 15"C, and only If. cI~okrcre and B. anrhracis were affected when the water was saturated with GO, (Scala & SanfcFicc 1891), When Pse~domonasfluorescens var. liquefaciens, Eschericlria coli var. cammr~nis, Staph. aurcrts, Sdm. typhi and V. cholesue were inoculated into carbonated waters, killing as inhibition could be effected, the extent depending upon the organism and intensifying with lime (Slarer 1893). Reduction of pathogenic organisms, but not sterilization, could be obtaincd in carbonated beverages (Young & Sherwood t91 I) , the bactericidal action of C02 being assumed ta be due to the increased hydrogen ion concentration of the solutjon (Koser & Skinner 1922; Valley & Rcttgcr 1927). Latcr cxperimcntal dala (Bcckcr 1933 ; Hays et a!. 1959), however, indicated that CO, per se, rather than its eflect on pH, was the cause 01 the inhibitory erect (Table 1).

The dtclinc in cell numbers or E. coli and Salm. ~ypl~i in artificially inoculated, carbonated beverages, was apparently proportional to the plessure and storage time (Donald et at 19241, and nppatcnl sterilization was achieved in only a fcw instances. When E. cali was subjected to 350 atm of CO, Ihe number of bacteria was reduced by approximately one hall in 20 mjn (Swearinger & Lewis 1933). More recently the aerobic growth rate of E. coli in led-batch cultures was found not to bc inhibited by 0-2 atm KO, , mcasurtd in the emuent gas, but 17% and 2 1 % inhibition of growth rate was observed respectively at KO, = 0.64 atrn in complex medium and pCO, = 0-62 atm in defined medium (Mori el a!. 1983). In the same sludy, inhibition or thc growth satc ot Candidn brassicne was not observed until thc KO, in the emucnt gas was 0.6 1 a m . During anaerobic growth of E. coli the optimum growth rate was at a dissolved C 0 2 conccnlration of 1-3 rnmolll (xO.115 aFm pCO, in the gix phase), above which the growth rate was inhibited (Lacoursierc et nl. 1986), The perhaps not unexpected conclusion that was drawn from this, was that the maximum growth rate or E. coli occurs at CO, concentrations close to that found in the mammalian ~ u t , where E . coli naturally resides.

The spoilage microflora OF carbonated beverages are dominated by yeasts, and the carbonation tolerance of somc of thcse was rccenlly invcstigatcd (Ison Rc Guttcridgc f 987). The most tolerant yeasts or those studied were D ~ k k e r a nnornala and those of the genus Bresianom~ce~, a finding which

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is in with Bre!tanomyccs spp. being the sole spoilage micro-organisms of salt drinks with high lcvelr (Ison & Cutleridge 19R7).

1 5. Treatment or dairy products with CO,

1 The bacteria1 count of milk could bc rcduccd by 50 atm of C 0 2 . but steriIization was still never obtained (Hoffman 1906). Milk kept under 10 a m or CO, remained in good condition for 72 h,

untreated milk curdled in 24 h. Increased pressures ol CO, delayed lactic fermentation but no noticeable effect of CO, was observed at atmospheric pressure (Van Slykc & Bosworth 1907). such Iindings Icd to a numbcr or studies on the possiblc antibacterial eflect ob CO, in other dairy

Experiments on the eKect of CO, o n buttes indicated that carbonation could not bc relied upon as a means of destroying bacteria present in cream and rendering such cream, or the butter made from it, safe for human consumption (Hunziker 1924). Similarly, carbonation could not be relied upon to improve the keeping qualily or to prevent flavour delerioration of !he resulting butter. If E l was made from unpasteurized cream, carbonated butter developed the usual bacterial flavour derects (Hunziker 1924). It was concluded that i f any appreciable benefit was to be obtained from thc carbonation of butter, j t would be necessary to store the butter in a CO, atrnosphe;e, although in tjme buttes stored in this way also developed undesirable flavours (Prucha er at. 1925). Carbonation of the cream, or of [he butler during churning, did not result in any benefit tojustify the use oTCO, in this way (Prucha el 01. f 925).

Carbonation of ice-cscam had no apprcciable effect on the bacteria within the ice-cream (Prucha er ot 1922; Rettger el a!. 1922). I t was demonstrated that CO, at atmospheric pressure had no bacle- riost at ic or bacreriocidal eFTect ,on organisms originalIy present in the ice-cream, or on Srreprococnts loctis, E. coli or B. cereus added to it (Valley & Rct tger 1927). No marked dilTercnces in viabiliiy csufd be discerned, and the slight variations favourcd the aerated products and not the CO,-treated products. In any event, after 7 weeks there was no difference in the CO, contenr of carbonated and and unca~bonated ice-cream due to the egress of the C02 by diffusion. Carbonation did not e n h a n ~ Ihe keeping qualily OF milk, nor-prevent rapid bacterial prolireration of the pre-existing flora, nor of Srrep. lactis, E. coli, Salm. typhi nor Sdm. hirscfifeldii inoculated into the milk (Va!?ey & Rettger 1927). Thus, although bacterial activities could be inhibited in the case 01 carbonated bevcrages, steriliza-

tion of water, milk or milk producls was nnot possible simply by carbonation, and this was the general conclusion or a number of reports reviewed by Valley (1928). The mrbonalion of beverages was successful because the beverages were kept in air-light containers under pressore. In order to inhibit thc bacterial activities in daisy products hjghcr pressures lhan those used in carbonated beverages, Tor which 4.8 atm were recommended (Donald er al. 19241, would be required (Psucha er a!. 1925). The pH of carbonated bevcragcs tcnds to be somewhat lower than that of milk, and since conditions causing inhibition are often synergistic, this wolrId have also contributed to the success with carbon- a ted bevcrages.

More recently, when milk was szirred under a headspace or 1 slim pC0, the pH fell to 6.0 and the CO, content increased to about 30 rnrnolfl. When this milk was subsequently held ai 4 or 7°C there was a psanaunced inhibitory eflect on Ihe growth of psychrotrophs, as compared with controls in air (Law & Mabbi tt 1983). I f I O6 bacteria/ml was taken to bc thc point when degradative changes in the milk become unacceptable, then the CO, treatment extended the possibfe storage time by abouf 3 d (at 4°C) or 2 d (a 1 7°C) Tor "or' quality milk and even Eanger lor 'good' quality milk. The CO, could cadly bc rcmoved berare pasteurization, although this was not necessary if t hc milk was For cheese or yoghutt.

lligh concenlrations of CO,, combined with low oxygen concenlrations. play an important role in !he ripening of blue chcesc. Penicillium roqucfirti i s mainly rcsponsjble lot the ripening of blue cheese. A5 blue chccsc ripens, its oxygen content dccrcascs rapidly, and the CO, cantent rises. These conditions are uniavourable to all moulds, but they tend to affect Pen. roql~tforti to a lesser extent than ofher species likely te bc present and able to grow at the salt concentration round in blue cheese


morn & Currje 1913: Foster cr nl. 1958). T t has bccn suggested that piercing the checse stirnu!ares the growth or this mould by allowing GO, to escape (Golding E937).

6. Ptexmation of meat and fish by CO, I Partly in view of the growth-inhibitory effects of C02 that had been observed in some mses above, attempts, which began at approximately Ihe same time as thc early work on the carbonation of water, were also made to preserve meat and fruit in an atmosphere of CO,. Beef could bc SO preserved for 18 d in hot summer weaiher with daytime temperatures up to 32"C, whilst mutton showed spoilage in a vcry short time (Kolbe f 882). It i s not known what the contribution of the pH was to this effect Pork and lamb which went bad in 10 d in air at 4-57~2°C remained free from spoilage far 3 weeks when stored in CO, (KillerSer 1930). Partial pressures of CO, in the atmosphere suppressed mould growth an meat (Moran ct al. 1932) and the growth of Pseudon~onus and Achrornobacrer spp. in nutrient 'broth at 0 and 4°C (Haines 1933). Further work showed inhibition of the growth of such organisms on ox-muscle as - f "C in 0.1 aim pC02 (Ernpcy & Scott 1939). The first practical use or modified atmospheres containing elevated levels oi CO, as a preservarive in the handling of fresh meat was in the shiprncnt of wltole chilled beef carcasses from Australia and Ncw Zealand to Britain in the 1930s. By 1938,26% of the beef from Australia and 60% or that from New Zealand was being shipped undcr CO, atmospheres (Lawrit 1974). The ability or high conkntrations of CO, ( >O-1 a[m) to retard the growth of the Gram-ncgative spoilage flora of mcat, paullry and fish, and in this way to prolong the shelt-lire, is now urell docurnentcd (Tabls 23 and modified atmosphere packaging has beeomc the subject of over 4000 scientific papers in the past halr decade (Lioutas 1988). Com- mercially the beneficial effects of C02 on the shelf-lire of meat are used most during prolonged storage in rcfrigcrated bulk containers (Taylor 1971; Dainty er 01. 1983). as well as for wholesale and retail packages (Molin el ot. 1983; Liout as 1988; Young el 01. 1988). Gas-packaging has also been applied commercially for poultry meat (Timmons 1976; Mead 1983) on an cxfensive scalc in the US (Hotchkiss 1988). In addition ta thc use of CO, in gas-packaging, CO, pellets have been used to chill poultry (Thornson & Risse 1971), lamb carcasses and bccf wholesale curs during shipment from thc packers to the retail trade (Smith er al. 1974).

6.1. INRIBITION OF THE GROWTH AND METABOLIShI OF FOOD-SPOILAGE

M l C R O - O R G A N I S M S

In general, the rate of bacteria! multiplication decreases, and the length of the lag phase increases, with increasing levels of CO, @.g. Tomkins 1932; Haines 1933) and Gram-positive species are more resistant to the effects of CO, than art Gram-negative species [Sutherland er al. 1977; Silliker &

Table 2. Examples of Iht use of CO, Tor the extension d t h c shell-lire of meat and fish

Foodstuff Selectcd rciertnas

Beer

Pork

Clark & k n t z 1972, 1973; Partman cr a!. 1975; Silliker a~ at- 1977: Suthcrland et a/. 1977; Christopher d at. t979a

Hufiman 1974; SiIEiker ef a!. 1977; Chrisiophcr er al. 1979b, 1980; Enlors e! al. 1980

Cured meats Smoked pork BIickstad & hlolin 1983 Frankfurters OgiEvy & Ayres 1951b, 1953; Blickstad & hlalin 1983

Poulrry OgiIvy & Ayrcs f 951 a; Gardner et 01. 1977; Sandct & Soo 197%; Mead 1983 Fish Coynt 1932; Stansby & Grifiths 1935; Banks er 01. I980

Cod Cogne 1933a; Jtnsen et aE. 1981 Herring Molin er al. 1983b Crayfish Wang & Brown 1983 Salmon Stier ~r a!. 198 I ; Fey 8 Regenstein 1982

The use of GO, Tor lhc prtvtn~ion of food-spoilage by micro-organisms and lht possible mechanisms or action art discussed in rhe texl.


\ ~ ~ l f e 1980; Slier el a!. 1981). These cflecls vary with the concentralion or CO, , incubation temperature, organism and water activity of the medium (Wodzinski & Frau'er 1961). Both aerobic

and growth rate were inhibited by CO, in fluoresccn t and non-fluorescent Pser~dornonas sPPl AIlerornenas ptrtrefdciens and Y ersinio enlerolitica, although the inhibition was incomplete (Gill & Tan 1980). The inhibition pattcrn was apparently biphasic for each organism, such that above a

pCO, a lurther increase in pCO, had a minor inhibitory effect, as in an earlier report on ps. ptlofescens (Gill & Tan 1979). I n contrast to such organisms, Acinetobacter (Gill & Tan 1980), Ps. onsrginosa (King & Nagcl 1975), Ps.fiagi, B. cereus and Strep. cremoris ((Enfsrs & Moliri 1980) all djsp]ayed a degree of inhibition by CO, that was more or less proportional to the CO, partial pressure over the entire C 0 , pressure rangc tested. The relative inhibitory cffect 01 CO, (RI) was defined as:

RT = [(r, - r,,,)/rJ x 100 (10)

where r, = the growth rate of the control culture, and r,,, = the growth rate ot the C0,-inhibitezed culture (Enfors Sr. Molin f 981). As the temperature decreased, the R l for Ps. jragi and B. cereus increased (Enfors & Molin 198 I), as was the c a e with most of the exampla above. The ratio or ihe RI : CO, solubility at the corresponding temperature was approximately conslant, and independent of lempera ture. Hence the increased inhibition by CO, at lawcr tcmpratures was explained as being due to increased CO, solubility, as opposed to incrcased susceptibility to CO,. Since the initial microbial activity on muscle foods is located at the surface, however, it is a gas-solid interface that is being dealt with rather ahan a population dispersed in a liquid medium (Finne 1982a). The tern- peralurc effcct may no1 thererore display the same characteristics for such an interracial phenomenon as for a liquid medium. Resulzs Irom a number of other authors were' treated in a similar lashion: the RI : concenttat ion or dissolved CO, was plotted against ternperaturc and similar concIusions were drawn (Ogrydziak & Brown 1982), although in this case a number of the figures were plots of only two or three points.

The inhibitory eficl a l CO, on Psctrdomonas spp. has been frequently studied [e.g. Clark & Lentr 1969 (several strains), King & Nagel 1975 (Ps. aeritginosa), Gill & Tan 1979 (Ps. Juorescens}, 1980 (fluorescent and non-fluorescen t strains), Enfors & Malin f 980 (Ps. fragi)] since !his genus contains some of the major spoilage organisms of proteinaceous loodstuffs. Many or the results differ, however, wilh respect to the shape OF the curve of growth rate versus C02 concentration. Explana- tions could be offered in terms of the erect of growth substrate or the inherent genctic differences betwen different species or strains. Some o i the discrepancies may also bc blamed on the application, in some cases, or rairly crude systems to measure the growth rate. All of the above exprimenls were carried out in batch cultures, where it was observed that the (maximum) specific gtowth rate of Ps. jrogi decreased as the: pCO, in thc cftluent gas was increased, However, results lrom continuous cultures revealed a shoulder (between 0.035 and 0- 12 a!m CO,) in the curve of maximum specific growth rate (calcuIated from critical dilution tales) vs. pCO, that was not seen in the batch growth rate determinations (Molin 1983a). In oxygen-limited cul lures ihe growth restricting effect of 60, was much more severe (Molin 1983a),

Organisms which were CO,-sensitive when grown aerobically were unaffected by C 0 2 when grown anaerobically, as were Enterobrrcrer spp. and Brac!~arhrix thmmasphacto (Gill & Tan 1980), suggest- ing that I he sites or CO, inhi biiien during aerobic growth are different from those during anaerobic growth. Jn general the partial pressures used iri determining the degree of inhibition by CO, on the growth

or the food-spoilage bacteria were between Q and 1 atm. When hyperbaric CO, pressures were used it was found far instance that the time required to reach a given aerobic (sic) coount was three times longcr in 5 atm pate C02 than In 1 atm CO,, and 15 times longer in 5 atm C02 than in air [Ellickstad et a!. 1981). Thcsc high partial pressures or CO, have a considerable effect in prolonging the shelf-lire or unsterilizcd foodstuffs, by virtue 01 the fact that they select the microflora in favour of Lacrobacillus spp. which are non-pathogenic (Shaw & Nichol f 969; Roth & Clark 1975) (thcst are the organisms that arc among the least scnsitivc to high values oTpCO,) and by rducing the growth rate of even thesc hcfobacillus spg. (Opilvy & Ayres 1953; Blickstad er al. 1981 ; Johnson et al. 1982;


BSicksrad & Molin 1983). Hence the preserving a c h n OF C02 is not so much due to the control of the total microbial poipula tion as to a restriclion ar the lypes of organisms which most rapidly cause delerioralion. The selection of thc Loerobocillur spp. is vicwcd Lo have an added benefit, at many lactic bacteria are known to excrt an antagonislic cffcct against other bacteria (Price & Lee 1970; Schrodcr el a!. 1980). Njsin, or course, is well known as an antibiotic secreted by arta in lactic acid bacteria (Fowlcr t t at. 1975; Hurst 198 1 F

6.2. CO z-KESISTANCE OF FOOD-RELATED BACTERIA

A number of attempts have been made to group different types of food-related bacteria with regard to their C0,-resistance (eg. Coyne 1933b; Sutherland et of. 1977; Gill & Tan 19803, but the mcrh0ds used to evaluate growlh rates werc relalivcly crude. A more recent study (Molin 1983b) determined (he r~istance to CO, of a number ot such rood-related bacteria. Or the orgmisms studied, the relative growlh-inhibilory effect or 1 atrn pCO, , as compared with the growth rate in air, was the highest ( > 75%) for D, cereus, Broctrotlrrix thermosphaclo and Aeromonas kydrophiSn, and lowest (29- 53%) Tor E. coli, Slr~p. jaecolis nnd Lacrobacillt~s spp. Under nitrogen the relafive inhibitory efict of 1 am p C 0 2 on growth rate was lower than Tor aerobic growth; under anaerobic conditions i t was highest for 8. cereus, A. hydroplrila and Y. frederiksenii (52-67%), and lowest Tor Y. enteror'itica, Broth. rherrnospfiocta and Lactobadl'lus spp. (8-26%). In 1 atrn pCO, X i rep. faecalis, Citrobacrer Jreurtdii and E. coli had the highest maximum specific growth rates, and Broch. rhcrmosphacta, D. ceTetrs and Staph. aureus the lowest.

6.3, CO1 IN 711s PREVENTION OF IFOOD SPOILAGE D Y CLOSfRlDIA

Allheugh 1 atm pCO, inhibikd the germination of L3. cereus spores. the same conditions stimulated the germination of spores of Closiridium sparogemes and Cl. perfring~ns (EnTors & Molin 1978a)c Germination of CI. sporogenes spores was inhibited slighlly at 4 atrn and almost completely at 10 aim, whereas germination oTCLpefiingens wasslightly stimulated at 4 atm, unafkcted at 10atm and stopped at 25 atm of pure CO, (Enfors & Molin 1978a). In addition to decreasing the ta te of spore germination, CO, has been shown to be lethal to certain clostridia (Hays et nl, 1959). T h e number or spores or CI. b~~ryrictrrn, CI. borlrlinurn and CI. sporogmes arc dccrcased after 42 d In thc prcsence OF 7.1 atm of CO,.

Toxin production by CI. boruiinum was delayed in 1 azm pCOZ when compared with that in 1 atm pN, nl atmospheric pressure (Doyle T 983). Increasing the pressure or CO, iurt her delayed the onset of toxin production, although production was not totally inhibited at 8-8 atm oTCO,. At high partial pressures, CO, was lethal to CI. borrrlinttrn, thc rate of decrcase af colony-forming units being dependent both upon the CO, pressure and the Ieogth of exposure to i t . However, 8 atrn pCO, did not serve as a fully antibotulinal agent (Doyle I983),

Thc cfkct or Cot-enriched a tmosphercs on the bchaviovr oT food-poisoning organisms in poultry products has received comparatively little attention. There was no significant difference between the erect of CO, and N, atmospheres, at 4 3 T , on the growth or eight strains or CI. perfiringens, although t hcrc was a slightly increased lag phase with two of thc strains under CO, (Parekh S: Solberg 1970). For one strain of Cl. perfringens incubated at 20°C thc lag phase was 3 1 h under 1 aim pN, and 68 h under I alm pCO, (Mead 19831, which suggests that clostridjal growth could at least be delayed by the presencc of CO, under marginal growth-(emperaturn conditions. In relation to chicken breast portions f atrn pCOz rnarkcdly reduced the growth rate of the micr~~rganisrns present (Gibbs & Patterson 1977).

6.4. PRORLEhIS ASSOCIATED WITH THE PRESERVATION OF MEAT B Y C O Z - ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ATMOSPHERES

The ability of modified atmospheres to preserve non-sterile foodstufi has been shown to increase with increasing pCO, . However, several workcrs indicate that the concentration or CO, which may

*

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be used for meat storage is limited by the surface browning that occurs when the pCO, exceeds 0.2 atm (Pohja et al. 1967; Ledward 1970; Silliker et al. 1977), although others do not agree (Seidman et 01, 1979). The browning was thought to result from mctmyoglobin formation (Brown & Mebine 1969; Ledward 1970; Adams & Huflinan 1972; Silliker er al. 1977) since surface browning does not occur in low-myoglobin-content foods, including seafoods (Coyne 1933a; Stansby & Grifliths 1935). This is of primary importance to the consumers who assume that an acceptable colour of the lean indicates freshness; for example the colour of pork chops changed from greyish pink to a less desirable brown- ish or tan colour as storage time increased (Adarns & Huffman 1972). However, the odour of pork chops became objectionable before they were rejected because of appearance (Spahl et al. 1981)!

One way in which the development of the detrimental effect of CO, on the colour of meat may be circumvented by the addition of CO to the atmosphere, or by pretreatment with CO before the meat is placed in the C0,-enriched atmosphere for storage (Silliker & Wolfe 1980). Because of safety considerations, however, CO in modified atmospheres has not yet been approved by the regulatory agencies for commercial use in the packaging of fresh foods (Finne 1982a). In most fresh red meat applications a mixture of gases is used and a number of combinations have been suggested e.g. 80% 0,/20% CO, (Georgala & Davidson 1970), 85-90% 0,/10-15% CO, (Clark & Lentz 1973), 75% C02/15% N2/10% 0, (Hotchkiss 1988). These gases and their concentrations should be tailored to the individual product, but for nearly all products this will be some combination of CO,, N2 and 0,. Nitrogen serves as a filler to keep the package from collapsing & CO, dissolves into the product (Hotchkiss 1988). Oxygen is used to maintain the bloomed colour of the meat (Young el al. 1988) and to inhibit the growth of anaerobic pathogens, but in many cases does not extend the shelf life (Hotchkiss 1988); CO, is added to inhibit the respiration of the product (Kadar 1980) in addition to the growth and metabolism of micro-organisms.

6.5. PRESERVATION OF SEAFOOD BY C 0 2 - ~ ~ ~ ~ ~ l ~ 1 ~ ~ A T ~ I O S P H E R E S

Carbon dioxide has also been found to be etTective in inhibiting the growth of the normal spoilage microbes of fish (Coyne 1932, 1933a, Finne 1982b; Parkin & Brown 1982; Tomlins et al. 1982), and modified atmosphere packaging, containing CO,, is presently used in the seafood industry for bulk shipments (Banks et al. 1980; Bell 1980; neals 1982; Wilhelm 1982). C0,-enriched atmospheres have also been effective in retarding microbial growth during refrigerated storage or retail packaged seafood products (Finne 1982c; Lannelongue et al. 1982a).

As most of our seafoods are still harvested from the wild, the microbial flora is usually diverse, with the majority belonging to the genera Pseudomonas, A cinetobacter, Moraxella, Flavobacteriunt- CytopAaga and Arrlrrobacfer, and will of course be alTected by the environment from which the seafood is harvested (i.e. regional and seasonal differences), physiological condition of the animal, time between harvest and arrival at the docks, onboard handling, etc. (Lee 1982).

Concern has been expressed, in terms of controlled and modified-atmosphere storage (Clark & Takacs 1980), with regard to the psychrotrophic Y. enterolitica, and Campylobacter fetus ss. jejtmi, since CO,-enrichment is in fact used for selective isolation of these organisms (Skirrow 1977). However, seafood has not been implicated in infections caused by these organisms (Lee 1982).

Further concern with modified atmosphere storage of seafoods was related to the possibility of toxin produclion by Cl. botuliirunr, especially the psychro~rophic type E, before the fish spoils (Stier et al. 1981; Eklund 1982a, 1982b; Post et al. 1985), as up to 0.9 atm CO, had no elfect on growth-or toxin production (Silliker & Wolfe 1980, Lee 1982). To overcome this problem, fish could be stored refrigerated in CO, up to the period of retail display and then transferred to air (Bell 1982). For pork and beef there was a residual inhibitory emect of the C0,-containing atmosphere after transfer to air (e.g. Silliker et al. 1977; Enfors cr al. 1979; Silliker & Wolfe 1980; Wolfe 1980; Spahl er nl. 1981), an effect that was also observed with poultry (Ogilvy & Ayres 1951a; Bailey et al. 1979; Silliker & Wolfe 1980).

While it may not be possible to prove that the potential contamination of fish, by Cl. botulinum toxin, stored in C0,-rich atmospheres does not exist, there is evidence that it may not present a significant risk provided proper sanitation and temperature controls are employed (Daniels et a!.


Neil M. Dixolr mtii Douglas B. KeIl 1985). The potential lor contamination could atso be reduccd by maintaining [he temperalure below 33°C (Schmidt el 01. 1961). Clostridjal growth and toxin production has been detected in fish stared in vacuum- and CO,-packages, but, in all instances, the fish was spoiled beyond hope of human consumption (Banner 1978). Until ralcly from botulism can be demonstrated, the use of packaging involving low oxygen concentrations cannot be recommended lor retail use (Wilhetrn 1982). However, even if the toxin is rormed, normal cooking operations will. inactivate i t (ticciardello e! 01. 1967).

Although GO, was effective in prolonging the shelr-Iife of fresh finfish [the most effective corn. binations ol gas were 1 aim CO, or 0-4 atm COI/0.6 atrn N, (Lannelonguc cf a?. 1982b)], the ratc or microbial growth in thc finfish arter the removal of the CO, paralleled the rate of growth in fish stored without CO, (nanks et a/. 1980). A residual inhibilory effect oa microbial growth due to storage in 0-8 atm C02 was dernonstratcd for cod fillets storcd in a modified atmosphere and then transrerred lo air at 4°C Wang & Ogydziak 1986). Tt was suggested that this residual effect was not due to retention or CO, at the surface or the fillezs but was probably due to the microbial emlogy or lhe sysfcm, Aner 7 d storagc, with CO,, Lactobaciffus spp. and Alteromonas spp. were predominant, and 6 d after transfer to air Pserrdomonas spp. were again dominant (Wang & Ogrydziak 1986).

pseudomonads, which are among the major spoilage organisms far seafood stored refrigerated in air (Shaw & Shewan 89681, were inhibited during storage in CO, (Enfors & Molin 1980; Gill & Tan 1979). One possibIe problem during the storage of non-sterile foodstuffs in elevated CO, atmospheres is that the spoilage flora may genetically adapt to high levels or CO,, as apGeared to be the case with Pseudomonas spp.-like strains isolated from rock cad (Johnson & Ogrydziak 1984). On rock cod fillets stored in 0.8 atm CO, at 4"C, iLacrobacillus spp. and an Aeromonas-like organism became the predominant organisms, whilst V. parohoenrolyrictcs, Staph. aureus or CI. bur ulinum lypc E wcre not isafated from fresh or modified almosphere stored fillets (Mokhele et a!. 1983). Similar results wcre obtained with herring fillets (Molin et aL 1983). The initial microflora of fresh herring was dorninatcd by corynclorms, Flauabacicriuni spp., Moraxella-like organisms and Psertdomortas spp. In air the spoilage flora was dominated by Pseudomonas spp. and Atoraxelfa-like organisms, whereas homo- fermentative Lacfobacillrrs spp were the only organisms isolated from herring fillets stored in 1 aim CO, at 2°C (Molin er ol. 1983).

I n addition to retarding microbial growth on scatoods, C02-enriched atmospheres are also e l k - tive in reducing the rate of aminc production within the seafood itseli(T3rown es al. 1980, Parkin et at. 1981; Johnson et a!. 1982; Watts & Brown f 982). Whether this is a direct effect on the rcdex activities sf the components of the respiratory chain leading to trimtthylamine N-oxide is nor apparently known,

7. Preservalion of fruits and vegefsbles by Cat

Much of the value or CO, treatment of fruits is due to the delay of their rotting by fungi but this is not completely attributable ro a direct influence on the fungal organisms, since K O 2 influences the physiologjcal conditions of the host tissuc itself (Smith 1963). CO, is not in genera1 as important a laclor in reducing the amount of fungal growth as is lowering the temperature (Brown 6922). Partial pressures of COz in the rangc of 0 2 - 0 5 atrn nonetheless provided a strong check to fungal growth at all temperatures [Brown 1922; Brooks ct al. 1932). In comparison with air, 1 atrn CO plus 0.5 atrn CO, , plus 0.23 atm O2 gave an X W Q % reduction of rot development in strawberries (From Botrytis cinerea), apples (Pen. expansum), lemons ( Whetrelinia sclerotiortrm) and oranges {Pen. iralicum and Pen. digitutum) {El-Goorani lk Somrner 1979). The eflectiveness of the CO, treatment depends, of course, upon r he amount or nutrient available to the lungus, and with greater retardation of fungal growth (due re CO,) at lower tcmperatures (Brown 1922; Moran er nl. 6932). The early literature concerning the effects oTCO,, including the prevention of fvngal growth, on the storage of a variety ot Fruits and vegetables has bcen reviewed by Smith (1963). The inhibitory effects of CO, have also been exploif ed in the Bijhi process Tor the preservation of grape juice (Jenny 1952). Morc recently Ihc use or modified atmospheres, containing COz, have been limited to the international movement of selected vegetables and rruits and for large-scale dorncst ic transport of apples, pears, citrus fruits and

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CO, inhibition 119

abbage ( ~ r e c h l 1980). ZafPV & Kader (1988) rcviowd [he use of modified atmosphere packaging for the storage of fresh producc.

I 8. Conlrol of the production of rcrmentd t d s and beverages using C02 I

i 1, has been indicated above that under appropriate conditions CO, can preserve roods by virtue or its inhibitor)' influence upon certain food-spoilage organisms. However, the production of many ro,dsruffs of course act~ally relies upon fermentation processes (Piaas 1976, Rose 1981, 1982; Erichszn 1983; hlarshall 6? Law 1984; Campbell-Platt 1987). Thus, CO, may also be uscd as a means by lvhich to control ot affect the propcrtics or foods produced by termen tation. An example of this is the use of exogenous CO, as a conrrofling agent in the production or alcaholic beverages by the brewing industry [Hoggan 1980). The final concentration of many flavour compounds and esters may be def rcased by increasing the C02 pressure during fesmentalion (Drost 1977). The fermentation rate, the rate and extent of yeast growth, and the final conccnlration of fuse1 oils are all decreased by increasing COz ptessure, whilst the final pH is increased (Kunkee 8-i Ough 1966, Jones & Greenf cld 1982; Arcay-Ledezrna 8 Slaughter 1984).

~ermentation of malt extract medium by Saccl.rtlaromyces cerevisiae under a CO, pressure of 1-97 aim resulted in a changed pattern of absorption of amino acidsein the first 4 h, with a general excretion of amino acids therearter (Slaughter er al. 1987). Growth o i Sacch. ccrcvisiae was almost oompletely stopped by 2-7 atrn or CO, , but no changes in growth rate were observed in 2.7 atm of N, (Norton & Krauss 1972). At much higher pressures, 01 some 41 alm, inhibition of the growth rate of many organisms occurs. as demonstrated with Sirep. Jaecnlis at high hydrostatic pressures and high partial prcssute of inert gases, including nitrogen (Fenn & Marquis 1968). Inhibition of cell division and or the production of new buds by Socch. c~rctlisiae was caused by CO, when i t is produced endogenousty or added. In contrast, metabolic production or C02 was unaflected by endogenously-produced pressures which inhibited thc ccll division or this organism. Although cell division was inhibited, doubling of zhe DNA content of the cells still occurred, indicating that the inhibition or cell division was not due to the inhibition 01 DNA replication (Norton & Krauss 1972). Despite the increase in DNA conlent of the cells the cantent of RNA and protein per cell decreased (Lumsden e l a!. 1987). ATter onc hour at elevated COP pressures the mean cell valtlme or Sacch. cmecisioe had increased, whereas the mean cell volume of Schizosal.t.harornyc~s pornbe had decreased, svggesiing that Ihe influence of C02 upon cell characterjstics may be associated with a change in cell volume (Lumsdcn ct al. 1987). T h e effects oS CO, on Scltiz. pombe were otherwise the same as the cTfects of CO, on Sacch. rerevisine. The inhibition of cell division by CO, has also been observed in algae. Alter 8 h in 5% C02 in air Cl~lordla spp. did not reveal any internal subdivision into daughter cells, despite being shown to bc capable of division (Sorokin 1962).

9. Inhibition of other industrial ferrnentstion prmesses by Cot

The use of CO, Tor the conlrol of fermentation end-products is not rcstrictcd to [he brewing industry, and indeed there are many examples in which CQ1 can affect the progress or industrial termentations (Table 31, for good or for ill. CO, pressures may significantly influence the regulation of microbial metabolism favouring biomass or product formation (Mudgett & Bajracharya 1979; Bajracharya & Mudgetr 1980).

9.1. EFFECTS OF CO2 ON THE PRODUCTION OF BIOMASS

Thc partial pressure of CO1 may be increased to scvcral atmospheres in some fermenters, but in some cases, for example pressure-cycle ferrnenlers such as the 'Prutcen' plant at Billingham, WK, the parlial pressure of CO, may fl vctua te over a substantial range. In thc case of the 'Pruleen' plant the 60, may change from some 0.45 atrn to 0.05 aim in 1 min (Vasey & Powell 1984); theCO, concentration

- -. -


Neil M . Dixorr a d Douglas B. Kd1 Tablc 3. A summary of some of the indus~rial rementation pro-

cesses that are inhibited by CO,

Produc~/process inhibited by CO, Selected rertrtnots

Biomass 'Pruteen" Baker's yeast

Solvents

Amino acids Arpinine Histidiae Glutarnic acid

Antibiotics Penicillin Tetracycline OIcandomyein Slrept ornycin

Methane

Degradalion of lign,no~llulosic wastes

Vasey Rt Pourll 1984 Chen & Gutmanis 1976

Kfei er at. I934

Akashi et at. 1979; Ilirose I986 Akashi P I (11. 1979; Hirose 1986 Hirose er al. 1968

Shibai et a/. 1973; Ishitaki et al. 1973

H o & Smith 1486 Tikhonov at of. 1983 Dylinkina el aF. 1973 Rylinkina t r 01. 1973

Hansson tg79 C

Drew & Kadam 1979; Mvdgeir & Paradis 1985

Thcse processes are discussed in detai! in the lext oTsection 9.

is at its highest close to the base of the riser, whcrc growth is the grcatest. Growth of the organism used for the 'Pruteen' process, hdelhylopr'tiltis me~hylotrophrts, was found to Ix sensitive to CO, , with the maximum specific growth rate decreasing from 0.5 to 0-15/h as the partial pressure or CO, increased horn 0.05 ta 0-4 atm. Above 0.29 atrn CO, the product specification changed and the carbon-lo-cell conversion decreased (Vasey & Powell 1984).

During biomass production with bakers' yeast, inhibition of the extent ol yeast growrh &low 0.2 atm pCO, in the gas phase was negligible, with slight inhibition at 0.4 atm and significant Inhibition at 0-5 pCO, (Chen & Gutmanis 1976). l n ihe case at ethanol production by Zymomonas mobilis biomass production is inhibited by 60, (Schreder el a!. 1934) and it was noted that nucleation, by adding diatomaceous carth, or additional stripping or CO, , increased the glucose uptake rate during the esrly stages of fed-batch fermentation (Rurrill et nL 1983). During continuous cultivation, at high dilution rales, biomass production was increased by as much as 100% when C02 was decreased from 1.46 atm to 0.095 atm {Nipkow et a!. 1985). Product yicld was not affected by CO, partial pressure, but the glucose uptake and ethanol production rates decreased as the partial pressure of CO, was decreased. Nitrogen sparging was found to seduce lag times considerably in batch cultures, probably because of the removal of CO, (Veerarnallu & Agrawal 1986). In this study, however, no noticeable trend in glucose uptake or c than01 production rates were observed when CO, was removed from the culture medium. hspite lhis the specific growth rate jncrcased by 15% and the cell mass yield increased by 12%, but the overall ethanol yield decreased by 5%. Production oTCO, was shown to lx directly couplcd with cthanol rorrnation but not necessarily with cell mass production, indicating a dccoupling or growth Srom cthanol produdion (VeeramaIlu & Agrawal 1986). I[ was noted that high KO, combined with high ethanol concentrations caused a change in the morphology 01 2. mobl!is, leading lo the appearance or extensive slime and granular layers around the cells (Doelle & McGregor 1983). Alteration of the cellular morphology has also been obtained with Strep. murans, the shape of which could be dictated by the ratio of 'CO,', in the form of bicarbonate, to K+ in the gsowt h medium (Tao et al. 1987). A high bicarbonate/K+ ratio produced spherical cells, whereas z he cells remained bacillary in medium wiih a low bicarbonaleJK + ratio.

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9.2. EFFECTS OF ON T I I E PRODUCTION OF BIOCIIEHICALS

J'Juring thc production or acetone and britanol by Cl. acetobutylicum, the butanol/acetone ratio i s significantIp changed at CO, pressures above 2.6 atrn, with the virtual clirnination or clhanol pro-

I auction (KIei el al. 1984)- b'iaximum solrent produdion by CI. acetobutylicunr, at the expense or cell growth, was found to occur at 1.7 atm and substrate utilization was inhibited with increasing pCO,.

I The ability to shiR the product distribution would allow thc fermentation plant manager to respond to changes in demand and prim. In contrast to the effcfects of CO, on the product ratios of Cl. acetohrrr~*fici~m, the partial pressure of CO, docs not noticeably influence I he fermentat Eon products of CI. buryricurn (van Andcl ei ab f 985).

During aerobic batch growth of Br~cibarrarium jlacum on glucose under coniralled gas phases, coZ mas ro~nd to affect amino acid production (Akashi er at. 1979; Hirose 1986). At aEE pCO, values c02 reduced the yield of histidine, produced by Brev-Jovtrn~, rvhllst nrginine displayed an optimal

at a pCO, aT 0-1 2 atm, above which the yicld decreased rapidly. In this instance, as in the case or the fcrrnentalion by CI. acetobulylicum, it is thus possible lo control the ratio or products by the use of CO2.

During glutarnic acid production by Brra laclofermenturn high partial pressures of CO, caused a decrease in glutamate production, sugar consumption and respiratory activity (Hirose et ol. 19683.

! High CQ2 tension also resulted in a decrease in product Formation in a nucleoside fermentation employing a mutant of B. subtilis (Shibai ei al. 1973). In the same Fermentation, the yield of iaosine was shown to bc independent or the bicarbonate ion concentration in !he culttrre medium, but greatly reduced by increasing partial pressurw of C02 (Ishizaki et at 1973).

The production of antibiotics i s inhibited by relatively low partial pressures OF CO,. n c rate of synthesis of penicillin by Pen. chrysogerrum was halved by a CO, partial pressure or 0.08 atm (Pirt & Mancini 19751, when compared with the rate of synthesis at 0.00M.007 atrn pCO, . Exposure to influent gases of 0.03 and 0.05 atm or CO, produced no observable inhibition of the metabolism ot Pert. chrysogenunr, but influent gases of 0.126 and 0.2 arm of CO, inhibited both growth rate and penicillin production rate (Ho & Smith 1986). Tetracycline biosynthesis was found to be optimal at 0.02 atm CO, (Tikhonov er a!. 1983) and the inhibition by CO, of the production or othcs antibiotics, such as oleandomycin and streptomycin, have also been reported (Bylinkina el a!. 1973).

9.3. EFFECTS OF C 0 2 ON THE TREAT MEN7 OF WASTES

Any inhibitory erect or CO, could be of great importance in methane production during the digestion or wastes, since the partial pressure of CO, could increase to several atmospheres in large digesters. In general, rapid inmeass in KO, resulted in rapid decreases in methane production and vice versa (Hanssan 1979). The rncihane yields were 20-30% higher at low values o l pCO, compared with those at I atrn CQ2 (Hansson & MoIin 1981). Combined with decreasing methane yields, as pCOr increases from 0 l o 1 atm, there is a progressive inhibition of acetate and propionate degradation, although sornc CO, was required for propionate degradation since the rate or degradation dropped rapidly below 0.2 atrn CO, (Hamson & Molin 1981; Hansson 1982). High pCQ, also decreased the temperature maximum at which bacterial acetate degradation occurred (Hansson 1982).

Conversion of lignoccllulosic wastes is also sus~eptible to inhibition by CO, ; increasing CO, pressure increasingly inhibits the rate and extent or degradation of lignin and nan-Iignin matcrials by Phaneruclraete cltrysosporium (Mudgett & Paradis 1985). Lignin degradation rates were also suppressed by high levels ol C 0 2 in the later stages of the iermcntation ca talysed by Aspergillus fumi- golw (Drew & Kadarn 1979). Both inhibitory and stirnulatory effects of CO, have been reported for a number of other fermentations (Mudgclt 1980). Et may be concluded therefore that in some cases GO, exerts s mntsolling influence upon microbial gtowth and metabolism which may be utilised l o t biolechnological purposes. I t is therefore gemanc to cnquire into some of fhe possible mechanisms whereby CO, exerts its inhibitory effects at the subcellular level.


NeiI M. Dixoj~ and Douglas B. KeII

10. Sites of act ion

1g.l. BIOLOGlCAL hlELI DRANES

As it has been noted above thar CO, may inhibit cell division and cause alterations in cell rnorphog, agy, glucosc uptake rates and amino acid absorprion, i t would be reasonable to suggest that such effects of CO, may be associated with changes in lhc function of the bialogica.al membrane. Indeed one or lt he factors implicated in contributing to the reason for thc growth-inhibitory effects of CO, has been the alteration of membrane proper tics (Sears & Eiscnkrg 1961). 11 was suggested that CO, intetats with lipids of the cell rnernbranc, decreasing the ability of the ccll to uptake various ions. 'Anacsthesia' (i.e. narcosis) caused by elevated Iewls of pCO, was proposed as a basis Tor the effect of CO, an the membrane during CO,-mediated growth inhibition, and the available li teratute on yeast was rcviewed (lanes & Greenfield 1982). Changs in the permeability of the cell membrane were also invoked in connection with a study OF the eflects of CO, on the germination of bacterial spores (Enfors & Molin f 97%). The inhibition was suggested lo bc due to an increase in fluidity, causing the disturbance of the adivity of a membrane-bound enzyme essenlial 10 the initiation of germinat ion. Alterafions in thc fatty acid conlent, and fluidity, of the yeasi cell rnernbtane at elevated pCO, levels wcre noted (CasEeIli el a!. 1969).

One theory of narcosis is that absorption or an 'anaesthetic agent' ink a biological membrane causes a hydrophobic region to expand beyond a certain critical size. This theory is lermed the critical volume hyporhcsis (Miller el a!. 1973) and is consistent with the observations that anaesthetics expand manolayers, bilaytrs and bulk solvents (Seeman 1972) and that hydrostatic pressure can in some cases reverse anaesthesia (Lever et at. 1971). Expansion of biological membranes at clinically significant concentrations of general anaesthetic is estimated to be o l the order of 0.4% (Lever el al. 1971). I t has been demonstnled that anamthetics disorder the lipid bilayer of the membrane (Jain et OF. 1975, Vanderkooi et al. 1977, Pang, el ol. 1980). Perturbations in membrane fluidity, caused by the disordering ol the lipid bilayer, are postulated to after the Cunc~ion of membrane proteins, resulting in thc changes that may be associated with anaesthesia (Chin el a?. 1976; Rofh 1980). The phase transition hypothesis (Lee 1976) suggests that lipids surrounding functional membrane proteins exist in a g l phase (as a lipid annulus) retaining proteins that rorm ion channels in an open state, and anaesthetics 4rneEl' this rigid lipid (Roth 1980). Regions in which lipids in the liquid phase coexist with lipids in the gcI phasc are termed Eareral phase separations (Trudell 1977) and are associated with funaional changes in membrane proreins, possibly modulating the protein conforma- tion through hydrophobic or electrostatic Interactions. Anaesthetics may reduce these lateral phase separations, thus altering the lunctional activity oT the proteins (Roth 1980). In tach of the above theories the anacsthetic is taken ta bc interacting with thc lipid portion of the

membrane, and these theorics are known as lipid theories or narcosis. 3n contrast with t htst theories are tht protein theorics of narcosis. Thcse latter theories proposed that narcosis is due to a direct erect of the anaesthetic upon membranc proteins (Richards cr 01. 1978; Franks & Lieb 1986). The degenerate perturbation hypothesis (Richards er ol. 1978) proposes that small molecules are distrib- uted in one sel of hydrophobic sites of appropriate dimensions within membtanc proteins, and larger molecules may bind to distinct sets 01 sitcs on the membrane proteins. In addition to his, molccuEes with srructvrall features similar to thosc of phospholipids will compete For the regions of the proteins that interact with phospholipids; the replacement of annular lipids by anaesthetic molecules then interferes with the function or the protein.

n-Alcohols behave as anaesthetics; their potency increases until a certain chain ltngth is reached, beyond which their biological activity ceases. The lipid theories state that this *cut-off in anaesthetic activity is due to a corresponding cut-off in the absorption of the alcohols (Ehat arc then longer than the specific chain length) into the lipid bilayer of the membrane, Howevtr, it has k e n demonstrated that the partition of alcohols into lipid bilayers continues long after their biological activity has ceased (Franks & Lieb 1986). This supports the view that it is the membrane proteins and not the lipid bilayers, that art thc target sites for anaesthetics. The general anaesthetic properties of the n-alcohoIs can be accounted for in terns of binding to protein target sites of circumscribed dimen-

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,ions: the levelling off in potency occurs when the site becomes full, and the cut-off point occurs when

the for anaesthetic activity falls below the aqueous solubility (Franks & Lieb 1986). Narcosis may also be caused by the action of CO, on the cytoplasm as well as on the plasma

membrane. During C02 narcosis of the filamentous alga, Nitella clacata, there is a gradual reversible sol-to-gel conversion of the cytoplasm, assumed to be associated with the carbamination of proteins (FOX 1981). Removal of CO, from the gas phase restores the sol state of the cytoplasm from its

gelled condition. Also involved in the narcosis of the cytoplasm is the exosmosis of water and electrolytes. The carbarnination and subsequent coalescence of enzymic proteins would presum- ably deprive them of their full function as catalysts (Fox 1981).

Reaction of amino groups, present on membrane proteins, with CO, will result in potentially positive ions (RNH:) becoming potentially negative ions (RNHCOO-) (Mitz 1979). This charge change causes a change in the surface potential and may selectively favour the transport of positive ions, whilst inhibiting the transport of negative ions across the membrane. In addition to this there

probably be a significant conformational change associated with the charge change, which lv~uld also affect the function of the protein.

The inhibition by CO, of the uptake of amino acids by membrane vesicles of E. cofi and B. subfilis was only one half that of the inhibition of growth, whereas the uptake of glucose by membrane vesicles of E. coli was unaffected by 100% C02 (Eklund 1984). This might be interpreted to mean that the main mechanism of CO, action is not associated with the biological membrane. Such an interpretation can now be seen to be incorrect when viewed in terms of the so-called metabolic control analysis (e.g. Kacser & Burns 1973; Westerhoff et.al. 19841, which is discussed in the next section.

10.1.1. The metabolic control analysis

The metabolic control analysis was originally formulated to describe the control of metabolic pathways. When considering the control of metabolic pathways it is traditional to ask the question 'which step is rate Iimiting?', when referring to pathway substrates or products. However, the question that should more properly be asked of a parameter is 'how rate limiting is it?, and it has become apparent that the appropriate formalism with which quantitatively to approach such a question is the metabolic control theory (see e.g. Kacser & Burns 1973; Kell & Westerhoff 1986a, b, Kacser & Porteus 1987; Westerhoff & Kell 1987, Kell et aL 1989). This theory derives from the general formalism of sensitivity analysis (Cruz 1973), in which the sensitivity of any variable to any parameter is expressed as a 'sensitivity coefficient' or a 'control coeficient'. The control coeflicient of an enzyme, which expresses in quantitative terms the degree to which it may be rate limiting to the flux through a metabolic pathway, is defined (e.g. Kell & Westerhoff 1986b) as

where Cf is the flux control coemcient of enzyme i, J is the flux through the pathway, e, is the concentration of enzyme i and ss denotes steady state. It should be noted that the differentials apply strictly to infinitesimal changes in the parameter and the variable studied, but, particularly to accom- modate values of the parameter equal to zero, it is permissible to use the (small but finite) values of the changes themselves (i.e. SJ, SeJ to calculate the control coeficients. The control analysis contains a number of other theorems relating system properties such as fluxes to the properties (the so-called elasticities) of individual enzymes. The metabolic control theory can be applied to processes other than flux through metabolic pathways, as in our work on the efiects of C02 upon the growth rate of CI. sporogenes (Dixon et al. 1987). Hence the above statement, that the main mechanism oTCO, action is not associated with the biological membrane, may be incorrect, as this mechanism will contribute to the overall effect of CO, on the cell. If the control coeficient on growth for a membra- nous enzyme (times the elasticity of the same enzyme towards CO,) is greater than that for any other similar interaction, then it will in fact be the 'main' mechanism of action. Further, the value of the

-


control coeliicient will tend 10 vary with (he environmental conditions, so in one set or conditions onc enzyme may exert the most control, but in another sct of conditions it may bc another enzyme that exerts the most control on the growth rate.

Ra# her than a generalized effect an membrane-located proteins, CO, may exert its influence upon a dl by arecting the rate at which particular reactions procced. One way in which this may be brought about is or course to cause an altcsation in the production of a specific enzyme or enymes, via induction or reprmsi~n of enzyme synthesis (Jones & Greenfield 1982; Sarles & Tabita 1983; Dewien & Leadbeater 1984; Dixon 1988). It was suggested (Wimpenny 19691, and evidence has since been obtain4 (Wood & StjernhoIm 1962; Wood & Utter 1965; Wimpenny 1969; Jones & Greenfield 19821, that the primary sites at which C02 exerts its effects are the enzymatic carboxylation and decarboxylation reactions, although the erects extend to enzymcs not necessarily involved in rarboxylation or decarboxylation reactions (Jones & Greenfield 1982).

Thcre have bccn a number of studies showing that CO, causes alterations in the rate or certain enzymatic reactions in bacteria, leading to the build-up or the concentrations of ccrtain metabolites. Thus, increasing [he concentration of C02 caused Ihc rate ot succinatc fqrnation by E. coli rar. conimunc to increase, the removal of CO, causing a decrease in the succinate concen [ration (Etsden 1938). pCO, values of 0.01 to 0-1 atm 3lTected the enzymes of Sclerotiurn rovsisii, musing a decrease in the suminarc dehydrogenase activity and significant increases in thc ismitrate Iyase, jsocitrate dehy. drogcnase, malate synthasc and malare dehydrsgenase activities, compared to when the organism was grown in air (Kritzman el a/. 1977).

10.2 1. C0,-controlled induction/rcprcs~ion of enzyme synthesis

The conlsol exerted upon the enzymes or Sclerotiurn rofiii, as mentioned above, was through induction/repression or enzyme synthesis. Similarly the control OF autolrophic CO, fixation by CO, is mostly by induction or repression of enzyme synthesis. When COr was supplied at low partial pressvrcs { = 0.02 at rn in hydrogen) to photolithotrophically grown cclls of RhodospfrilItrm rubrum, up to 50% of the soluble protein was ribulose 1,5-bisphospha te carboxylase/~~xyge.enase [RuRPCase); increasing the pCO, from 0.02 to 0.05 ntm resulted in a rapid and dramatic decrease in the rate and cxtent of RuBP synthesis. LowetEng the C a t back to 0.02 atm resulted in a dramatic increase in RwBPCase synthesis (Sartes & Tabita 1983; Tabita et nl. 1985). This rcsponsc to thc partial pressure of C02 appeared lo be typical e i other chemotrophic and phototrophic organisms, a1 though !hey may not be as sensitive to C 0 2 or synthesize the same amount of RuRPCase as Rho&. nrbrum (Sarles & Tabita 1983; Tabita et ah 1983,1984). COz limitation of A!coligenes elrtropl~us depresses the synthesis of RuBPCase and phosphoribulokinase (PRK) lo about one-fifth of the normal autotrophic level (Friedrich 1982; Bowien & Leadbeater 3984). RuBPCase i s activaled by CO, (Lorimer 1981a; Miziorko & Larimer 1983). The reversible acliva tion process is accompanied by a carbamatt forrna- tion at a specific activator site lysine on Ihc Iarge subunit of thc enzyme (Lorimer & Mfziorko 1980; Lorimer 1981b). Activation of RuBPCase from Ale. eutrophus was shown lo result in a significant change 01 lhc hydrodynamic propcrt ies of the enzyme. The inactive enzyme exhibited a sedimentation coeficienl, S,,, , or 17.5 S, whereas activation lowered this valuc to 14-3 S (Bowien & Gottschafk 1982). This alteration reflects major changes in the tcrtiary structure of the enzyme, in which the small subunits could have a crucial function. Far further information about the control or CO, fixation see also Tabita ( I 9811, Dijkhuizen & Harder (1984) and Rowien es al. (1987).

10.2.2. COZ inhibirion ojenzjme reactions

Another way in which C 0 2 may influence the rate oTa reaction is to inhibit or stimulate the reaction, rather ihan affecting the synthesis or the appropriate enzyme. Formate hydrogenlyasc of E roli was also inhibited by CO, (Swanson & Ogg 1969). Fumara!~ formation by RRizopus nigricatts was

ter an hi; s?" ID rat bo OP

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at the pyruvate mrboxylation step duc to the inhibition or oxaloacctare dccarboxylase activity by CO, (Forlcr & Davis 1949). Both malatc dehydrogenase and isocitrate dehydrogenase of Ps. aerud i~rosa were round lo be inhibited by CO, , but oxafoacelate decarboxylase, fumarasc, succina te dehydrogenase and cylochrome c oxidasc wcre unatrected, although a small amount of inhibition might have been undetected (King & Nagel 1975). Catalase activily was reversibly decreased by hall in 0.1 3 atrn pCOl (nrclskin & Ivanovn 1955), although the peroxidalic activity or the enzyme was

(Mitsuda E! dl. 1958). The extracted protease activity OF Ps. fraqi was inhibited by increas-

ing of CO, , wllereas in the case or Streprom~*ccs coespftosus the extracted protease activity exhibited an optimum pCO, of 0.4 atrn pCO, in argon as compared with i t s activity in pure argon Pichard ct aI. 1984).

l I. Mcchanisrns of CO, inhibition of microbial growth and metabolism

Despile numerous reports of the effects of C 0 2 on microbial growth and metabolism, a number of which have bcen discussed, the 'mechanism' of COI inhibition still remains unclear. From what has been wrilten above, a unitary mechanism of CO, inhibition sccrns out of the question. However, a number of possible explanations have been postulated.

In an anaerobic chemostat cul lure of Klebsiella aerogenes it was demonstrated that increased con- I

centrations of metabolically produced CO, eSSccted a lowering of Geld values (Teixeira de Mattos et al. 1984). CO, exerts an effect on both metabolism and the energetics of cell synthesis. In this case the ~raposed mechanism was one of a futile cycle, dissjpaling energy, siimulated by increased CU1 concentrations and involving carboxyla tion and decarboxylation reactions, the net result being ATP -, ADP + P, (Teixeira de Mat tos et nl. 1984 and see Fig. la). Such erects of CO, on grow? h energetics have been observed with other organisms. During the growth of Cl. sperogenes in 'g lucos~ limited' chemostat culture in a defined minimal medium in which this organism required C02 tor growth (Dixon el 01. 1987; Lovitz el aL 1987), CO, induced some type OF metabolic 'slip", since both t he yield coeficienl arrd Ehe apparent maintenance requirements decreased as the pCO, was increased above the optima1 pC02 (0.5 atrn) for growth rare in 'unrestricted' batch culture (Dixon er al. 1988; see also Pennock & Tempest 1988 for similar energetic behaviour in B. sssear~.orhermophilus). A futile cycJc stimulated by CO, and pH, involving the CO, /!KO; equilibrium was proposed as a possible mechanism of energy dissipation in the Farmer case (Fig, lb). The occurrence of tutile cycles wit1 have an increasing importance, to the cell. as the growth rate is decreased e.g. in nature.

A nun-equilibrium thermodynamic assessment of the 'etliciency of growth' of heterotrophic bacteria indicated that they havc in gcncral cvalvcd to pcrmit a maximum metabolic flux of the carbon- and energy-source a 1 the expense of emciency or yield, so that the thermodynamic eficiency of microbial growlh js low but optimal for maximal growth rate (WesterholTet a]. 1983; Kell 1987). When CE. sporogenes was grown in chemostal culture in a mcdiurn in which CO, was not required for growth (Dixon d a!. 1987; Levitl el al. 3 9871, as the pCO, was increased above the optimal pCQ, for growth rate in "unrestricted' batch culture, the thermodyn~mic eRciency of growth was increased (in that both yield (Y Fp) aqd maintenance requirements increased (sic)); thus the system was no longer optimal for maximum growth rate (Dixon el al. 1988).

Variation in the response to CO, with medium composition was observed in the case of Ps.$uores- tens (Tan & Gill 1982). If basic cell functions, such as protein synthesis, or reactions of central metabolic pathways wcrc the processes that became most rate-limiting for growth under CO,, then the pattern o l inhibition would be expected to be similar in the ditTerent media. As they were not it was necessary to postulate difTercn1 rale-lirniling reactions for each medium, I t was postulated that the inhibition of growth rate by CO, would depend on cithcr non-specific inhibition of enzymes jnvolved in the early stages or substraie utilization or the inhibition ol subslratc uptake. Indirect inhibition of enzymes, resulting from a decrease in intracellulas pH caused by C02 (Walk E980), was untenable as an explanation since decreasing the intracelIular pH by altering the medium pH actually stimulated growth (Tan & Gill 1982). The conclusion arrivcd at was that the inhjbitory action or C02 was probably exerred at the level of subsirate uptake. A poinl in favour 01 this conclusion was the failure of other workers la detect an accumulation 01 metabolites during CO,-inhibited growth of Ps.

Neil M. Dixorr and DorigIas B. Kell

Sum: ATP - AOP 4- Pi

-k + + Fig. 1. Futile cycles, involving CO,, that have been proposed as possibk mechanisms of energy dissipation. (a) The Sutilt cycle proposed for h'kbsiella ocrogenes (Tcixeira de Maitos er a!. 3984) which involves PEP carboxylasc and PEP carboxykinasc and i s stimulated by CO, . (b) CO, irccly permeates the bjolagical membrane and once inside I he d l , COI may then reacl with water to fom bicarbonate ions and liberate protons. In an attempt lo maintain the internal pH, protons art actively transported from thcl e l l , rcsuIting in the dissipation or energy. T h e bicarbonate ions may be adively transporled from the cell, at a further mergetic cost, or may 'FtakTrom lhe e l l . As lthc hydration of CO, is revtrsibk, the hicarbonate ions may react with a proton to produce watcr and CO,, which is able to pcrmeate the membrane thus cornplcting the cyclc. 0, proton pump (ATP hydralase); e, HCO; pump or leak.

aeruginosa (King & Nagel 1935). an organism closely related to Ps.fluoresccns. Accumulation of some intermediate might be expected lo result from the inhibition 01 specific ca tabalic enzymes, but this would not occur if the growth rate was being determined by the tate of substrpte uptakc. However, metabolites might not accumulate due to increased metabolic flux through other pathways that d o not include CO, inhibited reactions. Addit ionally, substra tc uptake may bc cxpcded to contribute to the growth rate-limitation but not be the sole reason for srrch limitation (sec Dixon et al. 1987; Wafter er at. 1987).

During the storage of proteinaceous roads in modified atmospheres containing CO, , the interaction of CO, is achicved through solubititat ion and absorption of C 0 2 (Mjtsuda et at. 1975). Most probably, a major factor in the cficacy ot CO, lies in i t s ability to penetrate the bacterial membrane, causing intracellular pH changes {hickin & Thomas 1975; Turin & Warner 1977) of a greater magni- tude than would be found for similar cxteznal acidification, whjch can be effedively buff'ered by the organism. The pH changes induced by medium-to-high partial pressures of CO, in the storage atmospheres are suficient to disrupt the internal enzymatic equilibria (Wok 1980). Such inlcrnal pH changes may a f k t enzymes not otherwise involved with CO,, and in addition to this, as all decar- boxylaticln reactions appear to produce carbon dioxide in the COr,,,, form (Krebs & Roughton

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CO, inhibit iotl

1918; Detente er al. 1969) there is the possibility of feedback inhibition at elevaled pCO, . Reducing ,he temperature would serve to enhance this function by increasing the solubility of Cot.

Mutants of E. coli, Neerospora Ctassa and Salm. typ/~inturiu?n that are specifically inhibited by CO, haye been isolated (Roberts & Charles 1970). Thest mutants are inhibited at CO1 concentrations rvhich stimuIatc CO,-requiring mutants and which do not inhibit the wild-type organisms, with the inhibition being relieved by the addition or specific growth substances; lor example, the CO, inhibition of s mct hionhe-requiring mutant of N. crassa is reversed by purines, and the C02 inhibition of a prototro~h of Em coli is reversed by methionhe or vitamin 8,, .

Carbon dioxidc may exert a direct influence upon enzymes by affecting their physico-chemical properties. The rate and extenl of solution of proteins In water may be increased by CO, , and in some cases insoluble proteins becomc soluble; this is reversible since thcy ptecipitaie out again upon

of the COX (Mil2 1957,1978). Hence CO, may be utilized to adjust the solubility of protcins during thcir separation and purification (Yanari et ab 1960). Changes in C02 tension may cause changes in !he rate of solution, absolult solubility, dissoeia tion af complexes, reactivity, stabilily, charge and configuration of proteins (Mitz 1978).

A property of CO, , men tiancd above, is that it has a high reactivity with amines (Edsall 1969). The react ion of COr with uncharged primary arnines is many times faster than with water, resuf ting in the

i [ormation OF a catbarnic acid (RNHCOOH), with difirent amines having different reaction rate constants. At equilibrium the amount OF carbarnate is small, as thl dominating reaction is the reaction with water, due to the relatively small concentrations of the protcfns and thc high concentration

I of water present. I As has been indicated CO, can react with amino acids, peptides and proteins of the cell. The i

i protein carbarnate can causc the rorrnation o l internal eIectrosratic attract ions or repulsions that

I could result in slructural changes (Mitz 1979). These interactions could be between separate partions of the protein, between sub-units of a protein complex, or between the protein and bound heavy metals (Mitz 1979). Chargc changcs due to the reaction of C 0 2 with amino groups, as mentioned above in t hc case of membrane proteins, could cause very important changes in thc properties 01 thc prolein, especially in the case of enzymes which depend upon the possession of a specific charge for their activity. It is these structural and charge changes that may be responsible for the abave-

I mentioned changes in the physico-chemical properties of proieins. caused by CO, . Alteration of the physico-chemical properties OF a protein has been demonstrated in the case of

haernoglobia (Kilmattin & Rossi-Bernardi 1973). CO1 attached to the amino group of the protein as a carbamate i s associated with structural changes or the molecule which decrease the afiaity for 02. The ability 01 CO, to modulate the activity of enzymes has been demonstrated on enzyrncs in situ, in the case of enzymes orcarbohydrate and fatty acid metabolism of rat liver (Hastings 1970; Lonporc et al. I974), as has the ability of CO, or bicarbonate to regulate enzyme activity in crude cell- [iactions, e.g. NADP+ -specific glycerol dehydragenasc (Lcgisa & Mattey 1986). Another exarnplc of this is the activation of RuBPCase by CO,, mentioned above, rcsulling in the alteration of the cnzyrnc's sedimentation coemcient (Bowitn & Gottschalk 1982).

12. Concluding remarks

Despite the large number of reports upon ihe inhibition by C 0 2 , which forms the basis of thc discussion abovc, there does not appear to be a dear undtrsf anding of the role of CO, in the growth and metabolism of any given organism. Systematic studies of thc effects or CO, on bacteria are thererore warranted. Such studies arc or importance in attempting EO understand: (1) the role of CO, in the preservation o i foodstuffs, (2) the control by CO, of fermentations of biolechnological importance, and (3) the production of fine chemicals sin reactions involving CO, ,

We are grateful to ihc BiottchnoIagy Directorate or the Science and Engineering Research Coundl, UK, tor financial support and to Jan Harris for proof-reading the manuscript, We thank John


Hedger and Gareth Morris for stimulating discussjons, and an anonymous rcfcrce for helpfuI corn- mcn ts.

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A Review by CU2 micro-organisms - DBK Groupdbkgroup.org/Papers/dixon_inhib_jab89.pdf · 6. Preserva!ion ol meat and fish by COI, f 14 6.1. Inhibition ol the growth and metabolism