LETTERSPUBLISHED ONLINE: 13 JULY 2009 | DOI: 10.1038/NGEO580

Lightning-induced reduction of phosphorusoxidation stateMatthew Pasek1,2* and Kristin Block1

Phosphorus is frequently the limiting nutrient in marine andterrestrial ecosystems, largely owing to its poor solubilityand slow movement through the rock cycle1,2. Phosphorus isviewed to exist in geological systems almost exclusively inits fully oxidized state as orthophosphate. However, manymicroorganisms use the partially oxidized forms—phosphiteand hypophosphite—as alternative phosphorus sources3–5, andgenomic evidence suggests that this selectivity is ancient6.Elucidating the processes that reduce phosphate is thereforekey to understanding the biological cycling of phosphorus. Herewe show that cloud-to-ground lightning reduces phosphatein lightning-derived glass compounds, termed fulgurites.We analysed the phosphorus chemistry of ten fulguritesretrieved from North America, Africa and Australia, usingmicroprobes and 31P nuclear magnetic resonance. Half of thefulgurites contained reduced phosphorus, mainly in the formof phosphite. The amount and type of reduced phosphoruswas dependent on the composition of the fulgurite sectionexamined: carbon-rich sections contained around 22% reducedphosphorus in the form of iron phosphide, whereas otherfulgurites contained between 37 and 68% in the form ofphosphite. We suggest that lightning provides some portionof the reduced phosphorus used by microbes, and thatphosphate reduction by lightning can be locally important tophosphorus biogeochemistry.

Lightning is a ubiquitous phenomenon on the Earth, striking thesurface at a rate of approximately 44 events per second7. Lightningis also very energetic—itmay dissipate up to 109 J per flash8, heatingsurrounding air to instantaneous temperatures in the range of105 K (ref. 9). These high energies place lightning as one of thefew abiotic phenomena capable of breaking the nitrogen–nitrogentriple bond, allowing recombination with O2 or atmospheric gases,usually to form NOX compounds10. Although P does not follownitrogen in its geochemical behaviour, the highly energetic natureof lightning causes distinct chemical changes to occur to phosphatespresent in the target soil.

As lightning strikes the ground, the target material undergoesrapid physical, chemical and morphological change. Electricalcurrent flows through the target material, following areas of highconductivity or moisture content, plant roots or other subsurfacefeatures. As this material is rapidly heated, temperatures mayexceed 2,500K, and resultant boiling produces voids and vesiclessurrounding the path of the lightning, allowing escape of volatiles.This rapid heating and release of volatiles produces a cylindricallyshaped glassy core, sometimes hollow, surrounded by a roughouter surface composed of both melted and unmelted grains. Thismaterial is known as a fulgurite.

We analysed the bulk P chemistry of ten fulgurites retrievedfrom localities in the United States, the Sahara Desert and

1Department of Planetary Science, University of Arizona, 1629 E. University Blvd, Tucson, Arizona 85721, USA, 2Department of Geology, University ofSouth Florida, 4202 E. Fowler Avenue, SCA 528, Tampa, Florida 33620, USA. *e-mail: mpasek@cas.usf.edu.

New South Wales, Australia (Table 1). Where possible, wecompared the P speciation with samples of the target soil in whichthe fulgurite formed. For the purposes of these analyses, we dividethese fulgurites into three different types according to physicalstructure and chemical composition. Details of our classificationscheme are found in Supplementary Information. Type I fulguriteswere formed in quartz sand and have extremely thin, glassy wallstypically surrounding a hollow inner void. Type II fulgurites areformed in clayey soils or in loess. Grey crusts surround glassy wallsaround a large central void in these fulgurites. Type III fulgurites areformed in caliche or calcic soils. The glass in Type III fulgurites isusually thick and comprisesmost of the fulgurite structure.

Five fulgurite samples clearly demonstrate the presence ofphosphite (HPO2−

3 ) as a carrier of P in bulk fulgurite extractsas shown by 31P NMR (Fig. 1). These fulgurites span the rangeof our classification scheme, indicating that phosphate reductionis a common feature during fulgurite formation, and occurs inseveral different soil types. The amount of reduced-oxidation-state

Table 1 |Abundance of reduced-oxidation-state phosphorusin each fulgurite.

Fulgurite Pi(ppm)

PPi(ppm)

P3(ppm)

P1(ppm)

% Preduced

Type

Lake County, Florida 240 60 90 BDL 23 ISaharan Desert 300 BDL BDL BDL — INew South Wales,Australia

250 BDL BDL BDL — I

York County,Pennsylvania

210 180 100 BDL 21 II

Greensboro,North Carolina

600 BDL BDL BDL — II

Western New York 570 BDL Tr BDL Tr IILa Paz County, Arizona 280 BDL 280 BDL 50 IIIGreat Salt Lake, Utah BDL BDL Tr BDL Tr IIIYuma County, Arizona 160 BDL 90 BDL 37 IIIClark County, Nevada 380 BDL 820 Tr 68 III

SoilYork County,Pennsylvania

350 120 BDL BDL —

La Paz County, Arizona Tr BDL BDL BDL —Lake County, Florida 400 BDL BDL BDL —

Abundances of P species in extracts reported as ppm by weight in the fulgurites, determinedby ICP-MS analyses (see Supplementary Information) and comparison with standards15 . Pi isorthophosphate, PPi is pyrophosphate, P3 is phosphite and P1 is hypophosphite. Tr is a detectionof a trace amount of a P compound, and BDL is below the NMR detection limit (about 10 µM).The type identifies the variety of fulgurite, as discussed in Supplementary Information. Theseabundances are accurate to within±10%.

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LETTERS NATURE GEOSCIENCE DOI: 10.1038/NGEO580

¬10¬5020 15 10 5

¬10¬5020 15 10 5

¬10¬5020 15 10 5

a

c

b

Figure 1 | 31P NMR spectra of fulgurite extracts. The scale is given in ppmdeviation from a standard frequency, which for phosphorus is a solution of85% H3PO4 set to 0 ppm. The peak at 8 ppm is hypophosphite (H2PO−2 ),at 6.5 ppm is orthophosphate (PO3−

4 ), at 4.2 ppm is phosphite (HPO2−3 )

and at−4 ppm is pyrophosphate (P2O4−7 ). The type of fulgurite (for

classification see Supplementary Information) is also denoted. a, LakeCounty, Florida, USA. Type I. b, York County, Pennsylvania, USA. Type II.c, Clark County, Nevada, USA. Type III.

P (hereafter, reduced P) in each of these fulgurites ranges from21 to 68% (Table 1). One sample also showed the presence ofhypophosphite (H2PO−2 ) as a trace carrier of P (Fig. 1c).

Two carriers of reducedPwere identified bymicroprobe analysesof fulgurites. Several small spherules of iron metal alloy are presentin the glassy matrix of a Type II fulgurite from York County,Pennsylvania, USA (Fig. 2a). These spherules are enriched up to11wt% P, and up to 1% Si and 0.6%Ni. There are strong variationsin Pwt% across single spherules, with enrichment of P in therims of the metal spherules. These metal spherules are the onlyidentified P carrier in this fulgurite, although trace P could bedetected throughout the silicate fraction of the fulgurite.

A very different carrier was found in a Type III fulgurite fromYuma County, Arizona, USA. This region (Fig. 2b) seems to be apartially melted calcite grain interspersed with a mottled, lightermaterial roughly 5–10 µm in width consisting of P (∼10–15wt%),Si (∼2–4wt%) and Ca (∼31–36wt%). As colour variations in theP-rich mottled area were on the micrometre scale, point analysescould not be used to determine the exact location of P; however,energy-dispersive X-ray spectroscopy measurements indicate thatit is associated with the brighter of the colours in the mottled area.Phosphorus is also dispersed in low concentrations throughout thefulgurite, but as this mottled grain seems to have melted, it is thelikely carrier of reduced P in this fulgurite.

We propose two possible routes to reduced P production fromphosphate: (1) the complete reduction of phosphate to a phosphideor Fe–P alloy, and subsequent oxidation by reaction with water, and(2) the reduction of phosphate to phosphite. Phosphide mineralssuch as schreibersite, (Fe,Ni)3P, have been previously reported in afulgurite found in Michigan11. The formation of this fulgurite wasaccompanied by extremely reducing conditions, as demonstrated

20 µm

50 µm

Silica glass

Groundmass

Void

P-richFe metaldroplet

Calcite

P-rich areas

Silica glass

a

b

Figure 2 | Backscattered electron images of reduced-phosphorus carriersin fulgurites. a, Fe–P metal alloy spherules in a fulgurite from York County,Pennsylvania. The groundmass is a silicate glass with varying amounts of Feand Al. b, Ca–P–Si oxide grain in a fulgurite from Yuma County, Arizona.The darker areas are primarily calcite; the lighter mottled areas containhigher levels of P (10–15 wt%).

by the presence of both iron metal and elemental silicon. Thesereducing conditions were linked to a tree root that combustedand effectively smelted the glacial till to form metal alloys. Thelocal oxygen fugacity (fO2

) varied across the fulgurite by severalorders of magnitude, dependent on proximity to the tree root.The formation of phosphides in this fulgurite was hence linkedto combustion of carbon-rich material12. It has been shown thatschreibersite will react with water to form phosphite as a primaryproduct13–16. Thus, the likely pathway that led to the productionof phosphite is reduction of phosphate to phosphide, followed bysubsequent alteration of the phosphide to phosphite during ourextraction process. We propose that this pathway is the sourceof phosphite in the Type II fulgurite, given the presence of smallFe–P spherules throughout the glass of the fulgurite. However, thereduction of the York County target material was less extreme than

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NATURE GEOSCIENCE DOI: 10.1038/NGEO580 LETTERS

MH

IW

WM

600 800

Log 10

f O2

1,000 1,200Temperature (°C)

1,400 1,600 1,800¬25

¬20

¬15

¬10

¬5

0

CaHPO 3 -->

CaHPO 4

Figure 3 |Oxygen fugacity diagram with phosphate–phosphite transition.The curves define the oxygen fugacity versus temperature buffers for themagnetite–haematite (MH) transition, the wüstite–magnetite (WM)transition and the iron–wüstite (IW) transition11. Data for CaHPO3 wereapproximated by taking the specific heat capacity of brushite,CaHPO4×2H2O, which is the dominant soil phosphate in alkaline soil30

that was the target material for Type III fulgurites, and modifying thestandard heat of formation at 298 K to match the solubility of CaHPO3 inwater. As such, these data are an approximation of the actual fO2

line forthe phosphate–phosphite transition.

the Michigan fulgurite11, as no silicides or other minerals indicativeof extreme reduction were identified. Furthermore, the similarityof the NMR spectra of the Type I fulgurite with the Type II (Fig. 1)suggests the source of reduced P in the Type I fulgurite was also aphosphide formed by a pathway analogous to the Type II fulgurite.Extremely reduced species have been reported in Type I fulguritesfrom the Sahara, primarily within bubble cavities17.

The other possible reduction pathway invokes the partialreduction of phosphate to phosphite. No reduced P oxides have everbeen reported as mineral species; however, simulations of electricdischarges in phosphate ash form phosphite at yields up to 11%in a reducing atmosphere18, and are sometimes accompanied byphosphine production19.We propose that this pathway is the sourceof reduced P for the Type III fulgurites, although in contrast tothese laboratory studies, natural lightning forms phosphite even inthe present oxidizing atmosphere, and the yields are much higher.Type III fulgurites lack ironmetal, and formed in organic-poor soil,suggesting that reduction to phosphides did not have a role in the Pchemistry of these fulgurites. Our thermodynamic studies show thatphosphate (as CaHPO4) can be reduced to phosphite (as CaHPO3)at about 2,000K and an oxygen fugacity of about 10−5 (Fig. 3).

No natural reduced-P phases of oxidation state intermediateof phosphides and phosphates have ever been reported beforethe present work. As P is scavenged by biological systems, ifreduced P is present in the environment then the ability touse reduced P would be evolutionarily advantageous. Indeed,many microorganisms are capable of using phosphite as theirsole P source4, using well-conserved metabolic pathways6, whichimplies that reduction of phosphate occurs through naturalprocesses. Although phosphorus is well known to participate insome redox processes, for example, reduction of phosphate tophosphine20,21, these processes are almost certainly biologicallymediated. Other P redox processes are clearly biological, such asthemarine production and degradation of phosphonates, which areorganic compounds with C–P bonds22–24. Given the importance ofphosphorus redox in the biogeochemical cycle of phosphorus, andthe impact of the phosphorus biogeochemical cycle on other keybiogeochemical cycles such as carbon25, the identification of abioticphosphorus redox pathways is clearly relevant to understandingthe biogeochemical cycling of the elements. Our work provides anatural, abiotic source of phosphite formedby terrestrial processes.

We estimate the amount of P reduced per year (P, in kg yr−1)using the following equation:

P= flightning×CGfulgurite×Psoil×%reduced×MF

where flightning is the number of lightning flashes globally per year,CGfulgurite is the cloud-to-ground fraction of those flashes that forma fulgurite, Psoil is the amount of P in soil, %reduced is the percentageof P reduced by a single lightning strike and is specific to land typeand the fulgurite formed (see Table 1) and MF is the average massof fulgurites formed per strike. From these data (see SupplementaryInformation), the amount of P reduced by lightning is tentativelyestimated 2,000–3,000 kg yr−1 × /÷10 across the land surface ofthe Earth (approximately 0.02 g yr−1 km−2). In regions frequentlystruck by lightning, this amount could be locally enhanced, up to0.8–2 g yr−1 km−2. Thus, reduced P from lightning is not likely tohave an important role in the global P biogeochemical cycle, asfluxes of P of major importance globally are about a factor of 105times these production rates2. However, reduced P from lightningcould have an important role in local environments such as regionswith frequent cloud-to-ground lightning.

An implication of the present research is that other high-energy events, such as large impacts, may also reduce phosphates.Phosphides have previously been reported in tektites26,27, which areglassy melts formed by impact, and the present research suggeststhat large impacts, or periods of heavy bombardment28 may havesignificant roles in altering global P biogeochemical cycles bysupplying substantial quantities of reduced P. Such processes mayhave strongly affected prebiotic chemical pathways1.

The reduction of phosphate requires high energies and issignificantly affected by the chemical composition of the targetmaterial. Identified sources of this reduced P in fulgurites includeP-rich iron metal spherules and Ca–P oxides. The identification ofa source of reduced phosphorus compounds provides a rationalefor the evolution of microbes capable of using reduced P as theirsole P sources. Lightning may affect the biogeochemistry of Plocally, and fulgurites provide a rare view of abiotic phosphorusredox geochemistry.

MethodsWhole fulgurite samples were broken perpendicular to the long axis and includedexternal and internal material. These samples were then placed in round-bottomedflasks and phosphorus was extracted from these powdered fulgurite samplesusing a solution of 0.025M Na4 EDTA following previous work29. We used5ml of solution per 1.5 g of fulgurite extracted. Two extractions were carriedout on fulgurites from Greensboro, North Carolina; La Paz, Arizona; WesternNew York; and the Sahara Desert; all other fulgurites were extracted once as theamount of available material was limited. Each solution was sealed with parafilmand stirred constantly for 3–7 days using a magnetic stir bar. Solutions werefiltered and then evaporated to a thin layer of salt, and subsequently rehydratedwith 2–4ml of a 1:1 solution of NaOH and D2O for analysis. The solution wasdecanted and placed in an NMR tube for analysis by 31P NMR. Parallel extractionswere carried out on local soil samples when available, and serve as a check ofour methods. Inorganic reduced-oxidation-state P compounds have never beenobserved in soil samples.

Samples were analysed using 31P NMR on a Varian 300 four-nucleus probeFourier-transform NMR spectrometer at 121.43MHz and 24.5 ◦C for 256–34,000scans following previous work13–15. Solutions were analysed by three separatesets of scans on the NMR with the best signal-to-noise ratio coming from thehighest number of scans (>20,000). The values in Table 1 are retrieved from thescan sets with >20,000 scans. Spectra were acquired in both 1H-decoupled andcoupled modes to determine P–H bonds. The peaks were identified on the basisof comparison to known standards and previous work15. Abundances of eachcompound were determined from repeat integration of peak areas, which showedvariance of 2%, and inductively coupled plasma-mass spectrometry (ICP-MS)analyses of extracts (see Supplementary Information). Integration of NMR spectracoupled with ICP-MS of standards and solutions has been shown to be quantitativeto±10%with respect to P species concentrations15.

Samples were also analysed by electron microprobe point analyses. Fulguritesamples were cut perpendicular to the long axis or path of the lightning strike

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LETTERS NATURE GEOSCIENCE DOI: 10.1038/NGEO580

using ethanol or isopropyl alcohol as a lubricant to minimize water introductionto the centre of the sample. The samples were mounted in epoxy, polished andcarbon-coated according to standard procedures, and analysed using a CamecaSX50 electron microprobe. Point analyses, X-ray maps and backscattered electronimages were obtained. A current of 20 nA and an accelerating voltage of 15 kV with20 s peak count times were used.

Received 17 February 2009; accepted 18 June 2009;published online 13 July 2009

References1. Pasek, M. A. Rethinking early earth phosphorus geochemistry. Proc. Natl Acad.

Sci. USA 3, 853–858 (2008).2. Benitez-Nelson, C. R. The biogeochemical cycling of phosphorus in marine

systems. Earth Sci. Rev. 51, 109–135 (2000).3. MacIntire, W. H., Winterberg, S. H., Hardin, L. J., Sterges, A. J. & Clements,

L. B. Fertilizer evaluation of certain phosphorus, phosphorous, and phosphoricmaterials by means of pot cultures. J. Am. Soc. Agron. 42, 543–549 (1950).

4. White, A. K. & Metcalf, W. W. Microbial metabolism of reduced phosphoruscompounds. Annu. Rev. Microbiol. 61, 379–400 (2007).

5. Schink, B., Thiemann, V., Laue, H. & Friedrich, M. W. Desulfotignumphosphitoxidans sp. nov., a new marine sulphate reducer that oxidizesphosphite to phosphate. Arch. Microbiol. 177, 381–391 (2002).

6. Metcalf, W. W. & Wolfe, R. S. Molecular genetic analysis of phosphite andhypophosphite oxidation by Pseudomonas stutzeri WM88. J. Bacteriol. 180,5547–5558 (1998).

7. Christian, H. J. et al. Global frequency and distribution of lightning asobserved from space by the optical transient detector. J. Geophys. Res. 108,4005 (2003).

8. Krider, E. P., Dawson, G. A. & Uman, M. A. Peak power and energy dissipationin a single-stroke lightning flash. J. Geophys. Res. 73, 3335–3339 (1968).

9. Uman, M. A. Peak temperature of lightning. J. Atmos. Terr. Phys. 26,123–128 (1964).

10. Noxon, J. F. Atmospheric nitrogen-fixation by lightning. Geophys. Res. Lett. 3,463–465 (1976).

11. Essene, E. J. & Fisher, D. C. Lightning strike fusion- extreme reduction andmetal-silicate liquid immiscibility. Science 234, 189–193 (1986).

12. Maramba, B. & Eric, R. H. Phosphide capacities of ferromanganese smeltingslags.Miner. Eng. 21, 132–137 (2008).

13. Pasek, M. A. & Lauretta, D. S. Aqueous corrosion of phosphide minerals fromironmeteorites: A highly reactive source of prebiotic phosphorus on the surfaceof the early earth. Astrobiology 5, 515–535 (2005).

14. Bryant, D. E. & Kee, T. P. Direct evidence for the availability of reactive, watersoluble phosphorus on the early earth. H-phosphinic acid from the Nantanmeteorite. Chem. Commun. 22, 2344–2346 (2006).

15. Pasek, M. A., Dworkin, J. P. & Lauretta, D. S. A radical pathway for organicphosphorylation during schreibersite corrosion with implications for the originof life. Geochim. Cosmochim. Acta 71, 1721–1736 (2007).

16. Bryant, D. E. et al. Electrochemical studies of iron meteorites. Phosphorusredox on the early earth. Int. J. Astro. 8, 27–36 (2009).

17. Parnell, J., Thackrey, S., Muirhead, D. &Wright, A. Transient high-temperatureprocessing of silicates in fulgurites as analogues for meteorite and impact melts.Lunar Planet. Sci. Conf. Proc. 39, 1286 (2008).

18. Glindemann, D., de Graaf, R. M. & Schwartz, A. W. Chemical reduction ofphosphate on the primitive earth. Orig. Life Evol. Biosph. 29, 551–561 (1999).

19. Glindemann, D., Edwards, M. & Schrems, O. Phosphine and methylphosphineproduction by simulated lightning—a study for the volatile phosphoruscycle and cloud formation in the earth atmosphere. Atmos. Environ. 38,6867–6874 (2004).

20. Gassmann, G., van Beusekom, J. E. E. & Glindemann, D. Offshore atmosphericphosphine. Naturwissenschaften 83, 129–131 (1996).

21. Glindemann, D., Bergmann, A., Stottmeister, U. & Gassmann, G.Phosphine in the lower terrestrial atmosphere. Naturwissenschaften 83,131–133 (1996).

22. Sannigrahi, P., Ingall, E. D. & Benner, R. Nature and dynamics ofphosphorus-containing components of marine dissolved and particulateorganic matter. Geochim. Cosmochim. Acta 70, 5868–5882 (2006).

23. Paytan, A. & McLaughlin, K. The oceanic phosphorus cycle. Chem. Rev. 107,563–576 (2007).

24. Quinn, J. P., Kulakova, A. N., Cooley, N. A. & McGrath, J. W. New waysto break an old bond: The bacterial carbon–phosphorus hydrolases andtheir role in biogeochemical phosphorus cycling. Environ. Microbiol. 9,2392–2400 (2007).

25. Karl, D. M. et al. Aerobic production of methane in the sea. Nature Geosci. 1,473–378 (2008).

26. Chao, E. C. T., Dwornik, E. J. & Littler, J. New data on the nickel-iron spherulesfrom southeast asian tektites and their implications. Geochim. Cosmochim. Acta28, 871–980 (1964).

27. Iverson, W. P. Corrosion of iron and formation of iron phosphide byDesulfovibrio desulfuricans. Nature 217, 1265–1267 (1968).

28. Schoenberg, R., Kamber, B. S., Collerson, K. D. & Moorbath, S. Tungstenisotope evidence from similar to 3.8-Gyr metamorphosed sediments for earlymeteorite bombardment of the Earth. Nature 418, 403–405 (2002).

29. Cade-Menun, B. J., Liu, C. W., Nunlist, R. & McColl, J. G. Soil andlitter phosphorus-31 nuclear magnetic resonance spectroscopy:Extractants, metals, and phosphorus relaxation times. J. Environ. Qual.31, 457–465 (2002).

30. Sposito, G. The Chemistry of Soils (Oxford Univ. Press, 2008).

AcknowledgementsThis research was financially supported by grant NNX07AU08G from NASA Exobiologyand Evolutionary biology. We thank D. Lauretta for use of laboratory space andequipment. Soil samples of York County, Pennsylvania, USA were provided byBen Eiben, and La Paz County, Arizona, USA soil by T. Boswell of Joshua TreeImports. The New South Wales Australia fulgurites were provided by A. Hutchisonof Gemworx OZ.

Author contributionsM.A.P. planned analyses, acquired and prepared samples, ran extractions and wrote thepaper. K.B. prepared samples and acquired and analysed data.

Additional informationSupplementary information accompanies this paper on www.nature.com/naturegeoscience.Reprints and permissions information is available online at http://npg.nature.com/reprintsandpermissions. Correspondence and requests for materials should beaddressed to M.A.P.

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