Due to the lack of an ozone layer in the Archean, ultraviolet radiation (UVR) reached early Earth's surface almost unattenuated; as a consequence, a terrestrial biosphere in the form of biological soil crusts would have been highly susceptible to lethal doses of irradiation. However, a self-produced external screen in the form of nanoparticular Fe(III) minerals could have effectively protected those early microorganisms. In this study, we use viability studies by quantifying colony-forming units (CFUs), as well as Fe(II) oxidation and nitrate reduction rates, to show that encrustation in biogenic and abiogenic Fe(III) minerals can protect a common soil bacteria such as the nitrate-reducing Fe(II)-oxidizing microorganisms Acidovorax sp. strain BoFeN1 and strain 2AN from harmful UVC radiation. Analysis of DNA damage by quantifying cyclobutane pyrimidine dimers (CPD) confirmed the protecting effect by Fe(III) minerals. This study suggests that Fe(II)-oxidizing microorganisms, as would have grown in association with mafic and ultramafic soils/outcrops, would have been able to produce their own UV screen, enabling them to live in terrestrial habitats on early Earth. Key Words: Archean—Biominerals—UVR—Protection. Astrobiology 16, 301–310.
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References
1.
American Water Works Association and American Society of Civil Engineers. (2012) Ultraviolet disinfection. In Water Treatment Plant Design, 5th ed., edited by RandtkeS.J. and HorsleyM.B., McGraw Hill, New York, pp 12.1–12.41.
2.
BekkerA., HollandH., WangP.-L., RumbleD., SteinH., HannahJ., CoetzeeL., and BeukesN. (2004) Dating the rise of atmospheric oxygen. Nature, 427:117–120.
3.
BelnapJ., BüdelB., and LangeO.L. (2003) Biological soil crusts: characteristics and distribution. In Biological Soil Crusts: Structure, Function, and Management, edited by BelnapJ. and LangeO.L., Springer, Berlin, pp 3–30.
4.
BishopJ.L., LourisS.K., RogoffD.A., and RothschildL.J. (2006) Nanophase iron oxides as a key ultraviolet sunscreen for ancient photosynthetic microbes. International Journal of Astrobiology, 5:1–12.
5.
BoltonJ.R. and CottonC.A. (2008) Mechanism of UV disinfection. In The Ultraviolet Disinfection Handbook, American Water Works Association, Denver, CO, pp 25–40.
6.
BormanC.J., SullivanB.P., EgglestonC.M., and ColbergP.J. (2010) Is iron redox cycling in a high altitude watershed photochemically or thermally driven?. Chem Geol, 269:33–39.
7.
ChakrabortyA., RodenE.E., SchieberJ., and PicardalF. (2011) Enhanced growth of Acidovorax sp. strain 2AN during nitrate-dependent Fe(II) oxidation in batch and continuous-flow systems. Appl Environ Microbiol, 77:8548–8556.
8.
CleavesH.J. and MillerS.L. (1998) Oceanic protection of prebiotic organic compounds from UV radiation. Proc Natl Acad Sci USA, 95:7260–7263.
9.
CockellC.S. (2000) Ultraviolet radiation and the photobiology of Earth's early oceans. Orig Life Evol Biosph, 30:467–500.
10.
CroweS.A., DøssingL.N., BeukesN.J., BauM., KrugerS.J., FreiR., and CanfieldD.E. (2013) Atmospheric oxygenation three billion years ago. Nature, 501:535–538.
11.
Dalle-DonneI., RossiR., GiustariniD., MilzaniA., and ColomboR. (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta, 329:23–38.
12.
DillonJ.G. and CastenholzR.W. (1999) Scytonemin, a cyanobacterial sheath pigment, protects against UVC radiation: implications for early photosynthetic life. J Phycol, 35:673–681.
13.
DipponU., PantkeC., PorschK., Larese-CasanovaP., and KapplerA. (2012) Potential function of added minerals as nucleation sites and effect of humic substances on mineral formation by the nitrate-reducing Fe(II)-oxidizer Acidovorax sp BoFeN1. Environ Sci Technol, 46:6556–6565.
14.
DonaldsonJ.A. and de KempE.A. (1998) Archaean quartz arenites in the Canadian Shield: examples from the Superior and Churchill Provinces. Sediment Geol, 120:153–176.
15.
EmmeneggerL., SchönenbergerR., SiggL., and SulzbergerB. (2001) Light-induced redox cycling of iron in circumneutral lakes. Limnol Oceanogr, 46:49–61.
16.
FarquharJ., BaoH., and ThiemensM. (2000) Atmospheric influence of Earth's earliest sulfur cycle. Science, 289:756–758.
17.
FinneranK.T., HousewrightM.E., and LovleyD.R. (2002) Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environ Microbiol, 4:510–516.
18.
Garcia-PichelF. (1998) Solar ultraviolet and the evolutionary history of cyanobacteria. Orig Life Evol Biosph, 28:321–347.
19.
GómezF., AguileraA., and AmilsR. (2007) Soluble ferric iron as an effective protective agent against UV radiation: implications for early life. Icarus, 191:352–359.
20.
HäderD.-P., and SinhaR.P. (2005) Solar ultraviolet radiation–induced DNA damage in aquatic organisms: potential environmental impact. Mutat Res, 571:221–233.
21.
HeglerF., PosthN.R., JiangJ., and KapplerA. (2008) Physiology of phototrophic iron(II)-oxidizing bacteria: implications for modern and ancient environments. FEMS Microbiol Ecol, 66:250–260.
22.
HesslerA.M. and LoweD.R. (2006) Weathering and sediment generation in the Archean: an integrated study of the evolution of siliciclastic sedimentary rocks of the 3.2 Ga Moodies Group, Barberton Greenstone Belt, South Africa. Precambrian Res, 151:185–210.
23.
HohmannC., MorinG., BrownG.E., ObstM., BenzeraraK., and KapplerA. (2010) Molecular mechanisms of As-binding to biogenic iron(III) (hydr)oxides precipitated by the nitrate-reducing iron(II)-oxidizer Acidovorax sp. strain BoFeN1. Geochim Cosmochim Acta, 74:A409.
24.
IlbertM. and BonnefoyV. (2013) Insight into the evolution of the iron oxidation pathways. Biochim Biophys Acta, 1827:161–175.
25.
JohnsonK.S., CoaleK.H., ElrodV.A., and TindaleN.W. (1994) Iron photochemistry in seawater from the equatorial Pacific. Mar Chem, 46:319–334.
26.
KapplerA. and NewmanD.K. (2004) Formation of Fe(III)-minerals by Fe(II)-oxidizing photoautotrophic bacteria. Geochim Cosmochim Acta, 68:1217–1226.
27.
KapplerA., SchinkB., and NewmanD.K. (2005) Fe(III) mineral formation and cell encrustation by the nitrate-dependent Fe(II)-oxidizer strain BoFeN1. Geobiology, 3:235–245.
28.
KapplerA., JohnsonC.M., CrosbyH.A., BeardB.L., and NewmanD.K. (2010) Evidence for equilibrium iron isotope fractionation by nitrate-reducing iron(II)-oxidizing bacteria. Geochim Cosmochim Acta, 74:2826–2842.
29.
KimJ.D., YeeN., NandaV., and FalkowskiP.G. (2013) Anoxic photochemical oxidation of siderite generates molecular hydrogen and iron oxides. Proc Natl Acad Sci USA, 110:10073–10077.
30.
KluegleinN. and KapplerA. (2013) Abiotic oxidation of Fe(II) by reactive nitrogen species in cultures of the nitrate-reducing Fe(II) oxidizer Acidovorax sp. BoFeN1—questioning the existence of enzymatic Fe(II) oxidation. Geobiology, 11:180–190.
31.
KluegleinN., ZeitvogelF., StierhofY.-D., FloetenmeyerM., KonhauserK.O., KapplerA., and ObstM. (2014) Potential role of nitrite for abiotic Fe(II) oxidation and cell encrustation during nitrate reduction by denitrifying bacteria. Appl Environ Microbiol, 80:1051–1061.
32.
KonhauserK.O. (1998) Diversity of bacterial iron mineralization. Earth-Science Reviews, 43:91–121.
33.
KonhauserK.O. and FerrisF.G. (1996) Diversity of iron and silica precipitation by microbial mats in hydrothermal waters, Iceland: implications for Precambrian iron formations. Geology, 24:323–326.
34.
LalondeS.V. and KonhauserK.O. (2015) Benthic perspective on Earth's oldest evidence for oxygenic photosynthesis. Proc Natl Acad Sci USA, 112:995–1000.
35.
Larese-CasanovaP., HaderleinS.B., and KapplerA. (2010) Biomineralization of lepidocrocite and goethite by nitrate-reducing Fe(II)-oxidizing bacteria: effect of pH, bicarbonate, phosphate, and humic acids. Geochim Cosmochim Acta, 74:3721–3734.
36.
MancinelliR.L. and McKayC.P. (1988) The evolution of nitrogen cycling. Orig Life Evol Biosph, 18:311–325.
37.
MeltonE.D., SwannerE.D., BehrensS., SchmidtC., and KapplerA. (2014) The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat Rev Microbiol, 12:797–808.
38.
MiotJ., BenzeraraK., MorinG., KapplerA., BernardS., ObstM., FérardC., Skouri-PanetF., GuignerJ.-M., PosthN., GalvezM., BrownG.E., and GuyotF. (2009) Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria. Geochim Cosmochim Acta, 73:696–711.
39.
MueheE.M., GerhardtS., SchinkB., and KapplerA. (2009) Ecophysiology and the energetic benefit of mixotrophic Fe(II) oxidation by various strains of nitrate-reducing bacteria. FEMS Microbiol Ecol, 70:335–343.
40.
OlsonJ.M. and PiersonB.K. (1986) Photosynthesis 3.5 thousand million years ago. Photosynth Res, 9:251–259.
41.
PantkeC., ObstM., BenzeraraK., MorinG., Ona-NguemaG., DipponU., and KapplerA. (2012) Green rust formation during Fe(II) oxidation by the nitrate-reducing Acidovorax sp. strain BoFeN1. Environ Sci Technol, 46:1439–1446.
42.
PatrickM. and RahnR. (1976) Photochemistry of DNA and polynucleotides: photoproducts. In Photochemistry and Photobiology of Nucleic Acids, edited by WangS.-Y., Academic Press, New York, pp 35–91.
43.
PfeiferG.P. (1997) Formation and processing of UV photoproducts: effects of DNA sequence and chromatin environment. Photochem Photobiol, 65:270–283.
44.
PhoenixV.R., KonhauserK.O., AdamsD.G., and BottrellS.H. (2001) Role of biomineralization as an ultraviolet shield: implications for Archean life. Geology, 29:823–826.
45.
PhoenixV.R., BennettP., EngelA., TylerS., and FerrisF. (2006) Chilean high-altitude hot-spring sinters: a model system for UV screening mechanisms by early Precambrian cyanobacteria. Geobiology, 4:15–28.
46.
PiersonB.K. and ParenteauM.N. (2000) Phototrophs in high iron microbial mats: microstructure of mats in iron-depositing hot springs. FEMS Microbiol Ecol, 32:181–196.
47.
PiersonB.K., MitchellH.K., and Ruff-RobertsA.L. (1993) Chloroflexus aurantiacus and ultraviolet radiation: implications for Archean shallow-water stromatolites. Orig Life Evol Biosph, 23:243–260.
48.
PlanavskyN.J., AsaelD., HofmannA., ReinhardC.T., LalondeS.V., KnudsenA., WangX., OssaF.O., PecoitsE., SmithA.J.B., BeukesN.J., BekkerA., JohnsonT.M., KonhauserK.O., LyonsT.W., and RouxelO.J. (2014) Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nat Geosci, 7:283–286.
49.
ReinhardC.T. (2012) Exploring the texture of ocean-atmosphere redox evolution on the early Earth. PhD thesis, University of California Riverside, Riverside, CA.
50.
SantosA.L., OliveiraV., BaptistaI., HenriquesI., GomesN.C., AlmeidaA., CorreiaA., and CunhaA. (2013) Wavelength dependence of biological damage induced by UV radiation on bacteria. Arch Microbiol, 195:63–74.
51.
SchädlerS., BurkhardtC., HeglerF., StraubK.L., MiotJ., BenzeraraK., and KapplerA. (2009) Formation of cell-iron-mineral aggregates by phototrophic and nitrate-reducing anaerobic Fe(II)-oxidizing bacteria. Geomicrobiol J, 26:93–103.
52.
SchmidG., ZeitvogelF., HaoL., InginoP., FloetenmeyerM., StierhofY.D., SchroeppelB., BurkhardtC.J., KapplerA., and ObstM. (2014) 3-D analysis of bacterial cell-(iron)mineral aggregates formed during Fe(II) oxidation by the nitrate-reducing Acidovorax sp. strain BoFeN1 using complementary microscopy tomography approaches. Geobiology, 12:340–361.
53.
SchwartzmanD.W. and VolkT. (1989) Biotic enhancement of weathering and the habitability of Earth. Nature, 340:457–460.
54.
SimpsonE.L., HenessE., BumbyA., ErikssonP.G., ErikssonK.A., Hilbert-WolfH.L., LinneveltS., MalendaH.F., ModungwaT., and OkaforO. (2013) Evidence for 2.0 Ga continental microbial mats in a paleodesert setting. Precambrian Res, 237:36–50.
55.
SinhaR.P. and HäderD.-P. (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci, 1:225–236.
56.
StookeyL.L. (1970) Ferrozine—a new spectrophotometric reagent for iron. Anal Chem, 42:779–781.
57.
StuekenE.E., CatlingD.C., and BuickR. (2012) Contributions to late Archaean sulphur cycling by life on land. Nat Geosci, 5:722–725.
58.
StummW. and SulzbergerB. (1992) The cycling of iron in natural environments: considerations based on laboratory studies of heterogeneous redox processes. Geochim Cosmochim Acta, 56:3233–3257.
59.
ThomazoC., AderM., and PhilippotP. (2011) Extreme 15N-enrichments in 2.72-Gyr-old sediments: evidence for a turning point in the nitrogen cycle. Geobiology, 9:107–120.
60.
van LisR., DucluzeauA.-L., NitschkeW., and Schoepp-CothenetB. (2011) The nitrogen cycle in the Archaean: an intricate interplay of enzymatic and abiotic reactions. In Nitrogen Cycling in Bacteria: Molecular Analysis, edited by MoirJ.W.B., Caister Academic Press, Norfolk, UK, pp 1–21.
61.
WangY., LinW., LiJ., and PanY. (2013) Changes of cell growth and magnetosome biomineralization in Magnetospirillum magneticum AMB-1 after ultraviolet-B irradiation. Front Microbiol, 4, doi:10.3389/fmicb.2013.00397.
62.
WatanabeY., MartiniJ.E.J., and OhmotoH. (2000) Geochemical evidence for terrestrial ecosystems 2.6 billion years ago. Nature, 408:574–578.
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