ISSN 0031�0301, Paleontological Journal, 2014, Vol. 48, No. 6, pp. 667–675. © Pleiades Publishing, Ltd., 2014.Original Russian Text © A.D. Temraleeva, M.V. Eltsov, V.A. Demkin, D.L. Pinsky, 2014, published in Paleontologicheskii Zhurnal, 2014, No. 6, pp. 93–101.

667

† INTRODUCTION

Recently, paleosol analyses of archaeological siteshave played a prominent role in the study of Holoceneenvironmental evolution of the Eurasian steppe. Paleo�sols buried under cultural layers, kurgan mounds,defensive earthworks, etc…, represent unique naturalobjects which preserved many features and propertiesthat reflect climatic, lithological, geomorphological,geochemical, biological, hydrological, and other con�ditions of their formation and development (Demkinet al., 2012). The study of the microbiological featuresof buried soils is an important goal in microbiology,paleoecology, and soil science, not only for the recon�struction of past events and ecosystems, but also toexpand our knowledge of the limits of survival and sta�bility of microorganisms. In recent years, data hasbeen collected on the features of microbial communi�ties from buried soils of up to several thousand yearsold under artificial constructions, kurgans and defen�sive earthworks (Demkina et al., 2000, 2004, 2009), aswell as paleosols buried as a result of natural processesunder alluvial, colluvial, and other deposits (Marfen�ina et al., 2009). However, these works concern bacte�rial (Khomutova et al., 2004; Demkinà et al., 2010)and mycological microorganismal assemblages(Kochkina et al., 2001; Marfenina et al., 2008;Sakharov, 2011), while soil cyanobacteria and algalgroups remain virtually unexplored. Thus, the aim of

† Deceased.

this work was the study of the algal flora of buried soilsand their modern analogs.

MATERIALS AND METHODS

The studied archeological site is located on the flattop of a drained, inter�gully watershed in the aridsteppes zone of the northern part of the YergeninskayaUpland (Volgograd Region) (Fig. 1a).

The climate of the region is temperate�continentalwith an average annual precipitation of 350–380 mm.The soil�forming rocks in the studied area are carbon�ate salinized loess loams. The natural vegetation is awormwood�sheep’s fescue association with a projec�tive cover of 40–80%. The vegetation is dominated bysheep’s fescue (Festuca sulcata), crested hairgrass(Koeleria gracilis), and wormwood, white (Artemisialercheana), Austrian (A. austriaca), and black(A. pauciflora). Based on archeological evidence, con�struction of the kurgan dates to the 1st century AD(Middle Sarmatian culture). The kurgan mound ismore than 1 m in height with a 40 m diameter. The siteis located in an arable plot.

Three buried soils were studied: non�solonetzicchestnut deeply solonchakous (D�779) and meadow�chestnut deeply salted (D�780) soils from the time ofkurgan construction, and a fine solonchakous solonetz(D�774) buried under a 30 cm thick soil�ground layernear the kurgan as a result of land reclamation in the1970s (Fig. 1b). The background chestnut deeply

Cyanobacteria and Algae of Buried Soils and Their Modern Analogues

A. D. Temraleeva, M. V. Eltsov, V. A. Demkin†, and D. L. PinskyInstitute of Physicochemical and Biological Problems of Soil Science, Russian Academy of Sciences,

Institutskaya ul. 2, Pushchino, Moscow Region, 142290, Russia.e�mail: temraleeva.anna@gmail.com

Received August 8, 2013

Abstract—Living green microalgae morphologically identified as Muriella terrestris and Heterochlorellaluteo�viridis have been cultivated from buried soil samples of a Middle Sarmatian kurgan (1st Century AD.).Paleosols for which the algal flora has been studied have a microalgal pool with a substantially lower abun�dance and taxonomic diversity than modern humus horizons. We discuss the probable reasons for the preser�vation of microalgae viability in paleosols over a period of 200 years after their burial. The first find of thegreen alga Hemiflagellochloris kazakhstanica in Russia was discovered in fine solonchakous solonetz, buriedapproximately 40 years ago as result of plowing of the kurgan. The structures of algal�cyanobacterial assem�blages of modern background soils are also considered.

Keywords: cyanobacteria, algae, buried soils, survivorship

DOI: 10.1134/S0031030114060136

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solonchakous soil (D�772) and the fine solonchakoussolonetz (D�773), assigned to the virgin site, served aspreviously studied paleosol analogs. Soil�algologicalsamples were taken in July 2011 from the A1 upperhorizon of buried and modern soils under sterile con�ditions.

Physicochemical soil analysis. Water�soluble car�bon content was determined by wet ashing accordingto the Tyurin method, and combustion according tothe Nikitin method (Sheudzhen et al., 2007). The totalamount of salts in the aqueous extract and the particle�size distribution were determined according to stan�dard methods (Arinushkina, 1961).

Algological soil analysis. Methods for mixed cul�ture growth were used to cultivate algae from the soils:the glass fouling method (Kuzyakhmetov and Dubo�vik, 2001) and water�soil cultivation (Temraleevaet al., 2011; Kostikov et al., 2001). Pure algologicalcultures were derived from mixed cultures and alsofrom a method of planting diluted soil suspensions.Algal and cyanobacterial monocultures were grown ina liquid agar nutrient medium BG�11 with and with�out nitrogen (pH = 7.0; agar 1%) at 23–25°С and a2000 lx illumination with a 12 hour photoperiod. Thestudies were based on visually noticeable algae devel�opment, manifesting in the form of spots “blooming”on the soil and appearance of “green” plaques andfilms, using light microscopy methods (bright�fieldand interference contrast) on Leica DM750 and CarlZeiss Axio Scope A1 (Germany) microscopes. Algalidentifications are documented by working drawings

and photomicrographs taken using color digital“Videozavr” (Russia) and Carl Zeiss MRñ 5 (Ger�many) cameras. Several in vivo cytochemical reac�tions were carried out under light microscopy: forstarch using Lugol’s solution; for the general mucusoutlines, a 1% mascara solution; for mucus structure,a 0.1% methylene blue solution; and for mucus col�lapse, 0.5–1% methylene blue solution. Monocultureobservation was up to 6 months. Various identificationguides were used for identifying algal species (Goller�bakh et al., 1953; Dedusenko�Shchegoleva and Gol�lerbakh, 1962; Ettl and Gärtner, 1995; Andreeva,1998; Komárek and Anagnostidis, 1998, 2005). In thiswork, we chose the algal system adopted in the inter�national electronic database AlgaeBase (Guiry andGuiry, 2013). The position of classes within orders andspecies within classes is given alphabetically. Cyanobac�terial and algal strains that were successfully monocul�tured were included in the algological collection ACSSI(Algal Collection of the Soil Science Institute).

RESULTS AND DISCUSSION

The characteristics of buried and modern soils arepresented in Table 1. In general, the humus horizon ofthe A1 paleosols (1st century AD) had a moderate�loamy particle�size distribution. Its thickness did notexceed 12 cm. This horizon was characterized by aneutral pH, a diagenetic accumulation of highly solu�ble salts, and a low humus content. The A1 horizon ofthe fine solonchakous solonetz (D�774), buried

20

15

10

5

25 m

Snf Snm C2sn C2 Cm

D�779

D�780

(a) (b)

Chir R.

Volga R.

L. Sarpa

Sal R.Don R.

Volgograd

N

0 100 km

20

15

10 5

20

20

2525

20

20

10

10

20

10

10

15

15

15

15

15

15

20

200 5 10 15

Fig. 1. Schematic map of the studied area: (a) geographical location of the studied object, (b) map of the buried soil cover(1st century AD). Soil index: (Snf) fine solonetz, (Snm) moderate solonetz, (C2sn) solonetzic chestnut, (C2) non�solonetzicchestnut, (Cm) meadow�chestnut.

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CYANOBACTERIA AND ALGAE OF BURIED SOILS 669

40 years ago, had low humus and soluble salt content,increased clay fraction content, and an alkaline pH.

The A1 horizon of modern soils (thickness around7–12 cm) had moderate�loamy particle�size distribu�tion, was characterized by a neutral pH, relatively highhumus content, and almost complete absence of solu�ble salts (Table 1). White wormwood�cereal � vegeta�tive association dominated the chestnut soil region(D�772) with a projected coverage of 70–80%; blackwormwood�cereal dominated the solonetz region(D�773) with a projected coverage of 40%.

The cyanobacterial and algal taxonomic content,isolated from background and buried soils, is pre�sented in Table 2. A single species of green algae wasidentified from each studied paleosol. The firstrecorded find of the Hemiflagellochloris kazakhstanicagreen algae (Figs. 2a, 2b) from Russia was discoveredin the buried solonetz (D�774). This genus and specieswere discovered and described by Watanabe and co�authors (Watanabe et al., 2006) based on the BAKg15strain isolated from the salinized irrigated soils of theIli River basin in Kazakhstan. Unicellular coccoidautospore�forming green algae were found in theremainder of the paleosols: Muriella terrestris in chest�nut (D�779) (Figs. 2c, 2d); Heterochlorella luteo�viri�dis in meadow�chestnut (D�780) (Figs. 2e, 2f). It ispossible that the preservation of viable Trebouxio�phyceae green algae in paleosols buried 2000 years agois linked to their small size (cell diameter of Muriella?terrestris and Heterochlorella? luteo�viridis is 2–3 and

5–7 µm, respectively), which increases the cells’ resis�tance to drought. According to Sakharov (2011), smallspores (d < 1.2 µm) dominated the fungal biomasscontent of buried humus horizons; their proportionvaried from 60% to 85% in paleohorizons. Large rest�ing structures, typically present in modern organo�genic horizons, were not found in buried soils. Kashir�skaya et al. (2010) found that proportion of microor�ganism cells smaller than 0.01 µm3 in volume is less inmodern soils than in sub�kurgan steppe soils. Addi�tionally, cell wall modifications of the Trebouxio�phyceae green algae Chlorella fusca, Chlorella vulgaris,Picochlorum eukaryotum, Prototheca wickerhamii,Pseudococcomyxa simplex have been described previ�ously (Atkinson et al., 1972; Geisert et al., 1987;Gross, 2000; Agrawal and Singh, 2001; Agrawal andManisha, 2007; Ueno, 2009). Their cell walls containsporopollenin, a biopolymer that is extremely resistantto chemical and biological degradation and ensuresthe preservation of pollen and spores in geologicaldeposits over the course of thousands of years. Thus,we can assume that the paleosol�isolated Trebouxio�phyceae green algae M. terrestris and H. luteo�viridis,buried 2000 years ago, could also contain this polymerin their cell walls and allow them to be preserved forsuch a long period of time.

Considerable cyanobacterial and algal diversity hasbeen found in modern analogs of buried soils (Table 2).Cyanobacteria dominated in the background solonetz(D�773): Microcoleus vaginatus (Fig. 3a), Nostoc

Table 1. Characterization of buried soils and their modern analogs

Parameter

Soils

modern buried

C2(D�772)

Snf

(D�773)Snf

(D�774)C2

(D�779)Cm

(D�780)

Time of soil burial – – 40 ya (1970s) 1st Century AD

pH 7.1 7.4 8.6 7.4 7.0

Humus, % 2.61 2.75 0.66 0.59 0.62

Amount of salt, % 0.05 0.04 0.05 0.51 0.63

Clay, % 29 24 32 28 30

Silt, % 10 8 17 10 10

Vegetative association White worm�wood�cereal

Black worm�wood�cereal

– – –

Projective cover, % 70–80 40 – – –

Soil index: (Snf) fine solonetz, (C2) non�solonetzic chestnut, (Cm) meadow�chestnut.

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TEMRALEEVA et al.

(a) 10 µm (b) 10 µm

(c) 10 µm (d) 5 µm

(e) 10 µm (f) 10 µm

Fig. 2. Micrographs of green algae from buried soils: (a, b) Hemiflagellochloris kazakhstanica aplanospores and zoospores;(c, d) Muriella terrestris vegetative cells; (e, f) Heterochlorella luteo�viridis vegetative cells and autospores.

microscopicum (Fig. 3c), Leptolyngbya nostocorum(Fig. 3d), Phormidium autumnale and P. papyraceumformed noticeable growths on the soil surface. Blen�nogenic Microcoleus and Nostoc are adapted to aridconditions because of their production of extracellularpolysaccharides which, due to their hydrophilic�hydrophobic characteristics, can take up and accumu�late water and so stabilize the cellular membrane dur�ing periods of desiccation (Grilli Caiola et al., 1993,1996; Potts, 1999; Tamaru et al., 2005). It is knownthat Leptolyngbya cyanobacteria from hypersaline anddry habitats produce mycosporine�like amino acids

(Rastogi and Sinha, 2009; Prasanna et al., 2010)which absorb ultraviolet light. Additionally, the fol�lowing cyanobacteria Leptolyngbya edaphica, cf. Pseu�danabaena frigida, Aphanocapsa incerta, Nostoc punc�tiforme (Fig. 3b), N. edaphicum (Fig. 3e), and the algaeMuriella terrestris, Pseudococcomyxa simplex (Fig. 3f),Klebsormidium flaccidum, and Eustigmatos olyphemwere encountered in this soil.

Compared to the solonetz, far fewer species werefound in the modern chestnut soil (D�772), and thesewere exclusively green algae. Amongst them, P. sim�plex and cf. M. homosphaera were predominant and

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CYANOBACTERIA AND ALGAE OF BURIED SOILS 671

(a) 10 µm (b)

(c) 10 µm (d)

(e) 10 µm (f)

10 µm

10 µm

10 µm

Fig. 3. Micrographs of cyanobacteria and algae from modern background soils: (a) Microcoleus vaginatus, (b) Nostoc punctiforme,(c) Nostoc microscopicum, (d) Leptolyngbya nostocorum, (e) Nostoc edaphicum, (f) Pseudococcomyxa simplex.

H. luteo�viridis was also found. A number of studiesshowed analogous patterns—the dominance ofcyanobacteria in the dry steppes soils of Kazakhstan(Novichkova�Ivanova, 2012) and in hypersalineaquatic ecosystems: Zabuye Salt Lake, Tibet, China(Zheng et al., 1985); Trapani saline lagoons, Italy(Margheri et al., 1987); Honda saline lake (Lopez�Gonzalez et al., 1998); Solar Lake (Abed and Garcia�Pichel, 2001); hydrothermal springs, Baja California,Mexico (López�Cortés et al., 2001); solar salterns,Eilat, Israel (Sorensen et al., 2004). Most of the spe�cies we identified were found in similar soil and envi�

ronmental conditions (Novichkova�Ivanova, 1980;Kuzyakhmetov, 2006; Vinogradova and Darienko,2008). It is likely that the absolute dominance ofcyanobacterial species over Chlorophyta in modernsolonetz is linked to a sparser projected vegetativecover than when compared to chestnut soil; this wasidentified by Vinogradova and Darienko (2008) as partof an algological study of Azov�Sivash National Park(Ukraine). Additionally, study of the Great Salt Plains(Oklahoma, USA) revealed that the ammonium formof nitrogen, and not the salinity, controls algal distri�bution (Kirkwood and Henley, 2006). In general,

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TEMRALEEVA et al.

Tabl

e 2.

Cya

nob

acte

rial

an

d al

gal t

axon

omic

con

ten

t of

mod

ern

bac

kgro

und

and

buri

ed s

oils

Ph

ylum

Cla

ssO

rder

Spe

cies

Soi

ls

mod

ern

buri

ed

C2

(D�7

72)

Sn

f

(D�7

73)

Sn

f

(D�7

74)

C2

(D�7

79)

Cm

(D�7

80)

Cya

nob

acte

ria

Cya

nop

hyc

eae

Nos

toca

les

Nos

toc

edap

hic

um–

+–

––

Nos

toc

mic

rosc

opic

um–

+–

––

Nos

toc

pun

ctif

orm

e–

+–

––

Osc

illa

tori

ales

Mic

roco

leus

vag

inat

us–

+–

––

Ph

orm

idiu

m a

utum

nal

e–

+–

––

Ph

orm

idiu

m p

apyr

aceu

m–

+–

––

Pse

udan

abae

nal

es

Lep

toly

ngb

ya e

daph

ica

–+

––

–

Lep

toly

ngb

ya n

osto

coru

m–

+–

––

cf. P

seud

anab

aen

a fr

igid

a–

+–

––

Syn

ech

ococ

cale

sA

phan

ocap

sa in

cert

a–

+–

––

Och

roph

yta

Eus

tigm

atop

hyc

eae

Eus

tigm

atal

esE

usti

gmat

os p

olyp

hem

–+

––

–

Ch

loro

phyt

a

Ch

loro

phyc

eae

Ch

lam

ydom

onad

ales

Hem

ifla

gell

och

lori

s ka

zakh

stan

ica

––

+–

–

Ch

loro

cocc

ales

cf. M

ych

onas

tes

hom

osph

aera

+–

––

–

Tre

boux

ioph

ycea

eC

hlo

rell

ales

Mur

iell

a te

rres

tris

–+

–+

–

Pse

udoc

occo

myx

a si

mpl

ex+

+–

––

Tre

boux

iale

sH

eter

och

lore

lla

lute

o�vi

ridi

s+

––

–+

Ch

arop

hyt

aK

lebs

orm

idio

phyc

eae

Kle

bsor

mid

iale

sK

lebs

orm

idiu

m fl

acci

dum

–+

––

–

Soi

l in

dex:

(S

nf )

fin

e so

lon

etz,

(C

2) n

on�s

olon

etzi

c ch

estn

ut,

(Cm

) m

eado

w�c

hes

tnut

.

PALEONTOLOGICAL JOURNAL Vol. 48 No. 6 2014

CYANOBACTERIA AND ALGAE OF BURIED SOILS 673

cyanobacteria are more resistant to increased soil saltcontent, marked fluctuations in humidity, high pH,and insolation (Stal, 2007). Halophilic and halotoler�ant cyanobacteria maintain an intracellular ion con�centration by accumulating dissolved organic com�pounds, while cyanobacteria that are less resistant tosalt stress use sucrose and trehalose for osmoregula�tion (Mackay et al., 1984; Reed et al., 1986). In con�trast to the wide spectrum of salt�tolerant cyanobacte�ria species, amongst green algae there are singular spe�cialist species (e.g., Dunaliella species) which flourishin hypersaline ecosystems.

CONCLUSIONS

(1) For the first time living, cultivable green algae,morphologically identified as Muriella terrestris andHeterochlorella luteo�viridis, have been found in paleo�sols buried under a kurgan mound (1st century AD).We believe that the preservation of their viability islinked to their small size and/or stability of their cellwalls.

(2) The green alga Hemiflagellochloris kazakhstan�ica has been found in Russia for the first time in solo�netz which was buried around 40 years ago as a resultof plowing of the kurgan.

(3) It has been established that the A1 humus hori�zon of modern background soils is characterized byconsiderable diversity of cyanobacteria and algae.Leptolyngbya, Phormidium, Microcoleus and Nostocfilamentous cyanobacteria dominated in solonetz,while Pseudococcomyxa and cf. Mychonast green algaewere prevalent in the chestnut soil. Such differences inthe algal�cyanobacterial assemblage structures couldbe linked to the density of grassy vegetation and phys�icochemical properties of the soil.

(4) Strains of cyanobacteria and algae which weresuccessfully monocultured were included in theACSSI algalogical collection.

ACKNOWLEDGMENTS

The authors would like to thank professorA.S. Skripkin, head of the archaeological expeditionof Volgograd State University, for help in the organiza�tion of fieldwork.

The work was supported by the Russian Founda�tion for Basic Research, projects nos. 14�04�31016,12�04�31685, and 12�04�00385.

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Translated by S. Nikolaeva