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Bacterial influence on the formation of hematite: implications for Martian dormant life

Published online by Cambridge University Press:  22 April 2021

Sudeera Wickramarathna Open the ORCID record for Sudeera Wickramarathna [Opens in a new window] ,
Rohana Chandrajith ,
Atula Senaratne ,
Varun Paul ,
Padmanava Dash ,
Saumya Wickramasinghe  and
Patrick J. Biggs Open the ORCID record for Patrick J. Biggs [Opens in a new window]
Sudeera Wickramarathna*
Affiliation:
Department of Geosciences, Mississippi State University, Starkville, Mississippi, 39762, USA
Rohana Chandrajith
Affiliation:
Department of Geology, Faculty of Science, University of Peradeniya, Peradeniya20400, Sri Lanka
Atula Senaratne
Affiliation:
Department of Geology, Faculty of Science, University of Peradeniya, Peradeniya20400, Sri Lanka
Varun Paul
Affiliation:
Department of Geosciences, Mississippi State University, Starkville, Mississippi, 39762, USA
Padmanava Dash
Affiliation:
Department of Geosciences, Mississippi State University, Starkville, Mississippi, 39762, USA
Saumya Wickramasinghe
Affiliation:
Department of Basic Veterinary Sciences, University of Peradeniya, Peradeniya20400, Sri Lanka
Patrick J. Biggs
Affiliation:
School of Veterinary Science, Massey University, Palmerston North4442, New Zealand
*
Author for correspondence: Sudeera Wickramarathna, E-mail: [email protected]
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Abstract

Previous exploration missions have revealed Mars as a potential candidate for the existence of extraterrestrial life. If life could have existed beneath the Martian subsurface, biosignatures would have been preserved in iron-rich minerals. Prior investigations of terrestrial biosignatures and metabolic processes of geological analogues would be beneficial for identifying past metabolic processes on Mars, particularly morphological and chemical signatures indicative of past life, where biological components could potentially be denatured following continued exposure to extreme conditions. The objective of the research was to find potential implications for Martian subsurface life by characterizing morphological, mineralogical and microbial signatures of hematite deposits, both hematite rock and related soil samples, collected from Highland Complex of Sri Lanka. Rock samples examined through scanning electron microscopy-energy dispersive X-ray (SEM-EDX) spectroscopy. Analysis showed globular and spherical growth layers nucleated by bacteria. EDX results showed a higher iron to oxygen ratio in nuclei colonies compared to growth layers, which indicated a compositional variation due to microbial interaction. X-ray diffraction analysis of the hematite samples revealed variations in chemical composition along the vertical soil profile, with the top surface soil layer being particularly enriched with Fe2O3, suggesting internal dissolution of hematite through weathering. Furthermore, inductively coupled plasma-mass spectrometry analyses carried out on both rock and soil samples showed a possible indication of microbially induced mineral-weathering, particularly release of trapped trace metals in the parent rock. Microbial diversity analysis using 16S rRNA gene sequencing revealed that the rock sample was dominated by Actinobacteria and Proteobacteria, specifically, members of iron-metabolizing bacterial genera, including Mycobacterium, Arthrobacter, Amycolatopsis, Nocardia and Pedomicrobium. These results suggest that morphological and biogeochemical clues derived from studying the role of bacterial activity in hematite weathering and precipitation processes can be implemented as potential comparative tools to interpret similar processes that could have occurred on early Mars.

Keywords

AnaloguesHematiteIron-metabolismMarsMicrobial coloniesMicrobial weathering
Type
Research Article
Information
International Journal of Astrobiology , Volume 20 , Issue 4 , August 2021 , pp. 270 - 284
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Allen, CC, Westall, F and Schelble, RT (2001) Importance of a Martian hematite site for astrobiology. Astrobiology 1, 111–123.CrossRefGoogle ScholarPubMed
Allison, L and Scarseth, G (1942) A biological reduction method for removing free iron oxides from soils and colloidal clays. Agronomy Journal 34, 616–623.CrossRefGoogle Scholar
Bell, J, Mcsween, H, Crisp, J, Morris, R, Murchie, S, Bridges, N, Johnson, J, Britt, D, Golombek, M and Moore, H (2000) Mineralogic and compositional properties of Martian soil and dust: results from Mars pathfinder. Journal of Geophysical Research: Planets 105, 1721–1755.CrossRefGoogle Scholar
Braun, B, Richert, I and Szewzyk, U (2009) Detection of iron-depositing Pedomicrobium species in native biofilms from the Odertal National Park by a new, specific fish probe. Journal of Microbiological Methods 79, 37–43.CrossRefGoogle ScholarPubMed
Cabrol, NA and Grin, EA (1999) Distribution, classification, and ages of Martian impact crater lakes. Icarus 142, 160–172.CrossRefGoogle Scholar
Cabrol, NA, Wynn-Williams, DD, Crawford, DA and Grin, EA (2001) Recent aqueous environments in Martian impact craters: an astrobiological perspective. Icarus 154, 98–112.CrossRefGoogle Scholar
Christensen, P, Bandfield, J, Clark, R, Edgett, K, Hamilton, V, Hoefen, T, Kieffer, H, Kuzmin, R, Lane, M and Malin, M (2000a) Detection of crystalline hematite mineralization on Mars by the thermal emission spectrometer: evidence for near-surface water. Journal of Geophysical Research: Planets 105, 9623–9642.CrossRefGoogle Scholar
Christensen, PR, Bandfield, JL, Smith, MD, Hamilton, VE and Clark, RN (2000b) Identification of a basaltic component on the Martian surface from thermal emission spectrometer data. Journal of Geophysical Research: Planets 105, 9609–9621.CrossRefGoogle Scholar
Christensen, P, Morris, R, Lane, M, Bandfield, J and Malin, M (2001) Global mapping of Martian hematite mineral deposits: remnants of water-driven processes on early Mars. Journal of Geophysical Research: Planets 106, 23873–23885.CrossRefGoogle Scholar
Clark, BC (1998) Surviving the limits to life at the surface of Mars. Journal of Geophysical Research: Planets 103, 28545–28555.CrossRefGoogle Scholar
Climate-Data.Org (2020) Kandy Climate (Sri Lanka) [Online]. Available at https://en.climate-data.org/asia/sri-lanka/central-province/kandy-5671/ (Accessed 2020.07.28 2020).Google Scholar
Cornell, R and Schwertmann, U (1996) The Iron Oxides. Weinheim: VCH.Google Scholar
Croal, LR, Gralnick, JA, Malasarn, D and Newman, DK (2004) The genetics of geochemistry. Annual Review of Genetics 38, 175–202.CrossRefGoogle ScholarPubMed
Crosby, HA, Roden, EE, Johnson, CM and Beard, BL (2007) The mechanisms of iron isotope fractionation produced during dissimilatory Fe(III) reduction by Shewanella putrefaciens and Geobacter sulfurreducens. Geobiology 5, 169–189.CrossRefGoogle Scholar
Esther, J, Sukla, LB, Pradhan, N and Panda, S (2015) Fe(III) reduction strategies of dissimilatory iron reducing bacteria. Korean Journal of Chemical Engineering 32, 1–14.CrossRefGoogle Scholar
Feyh, N and Szewzyk, U (2010) Desiccation tolerance of iron bacteria biofilms on Mars regolith simulants. Geophysical Research Abstracts 12, 15204.Google Scholar
Flemming, H-C and Schaule, G (1996) Measures against biofouling. In Heitz, E, Sand, W and Flemming, H-C (eds). Microbially influenced corrosion of materials – scientific and technological aspects. Berlin and Heidelberg and New York: Springer, pp. 121–139.CrossRefGoogle Scholar
Fredrickson, JK, Zachara, JM, Kennedy, DW, Dong, H, Onstott, TC, Hinman, NW and Li, S-M (1998) Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium. Geochimica et Cosmochimica Acta 62, 3239–3257.CrossRefGoogle Scholar
Gao, L, Lu, X, Liu, H, Li, J, Li, W, Song, R, Wang, R, Zhang, D and Zhu, J (2019) Mediation of extracellular polymeric substances in microbial reduction of hematite by Shewanella oneidensis MR-1. Frontiers in Microbiology 10, 575.CrossRefGoogle ScholarPubMed
Gilichinsky, D and Wagener, S (1995) Microbial life in permafrost: a historical review. Permafrost and Periglacial Processes 6, 243–250.CrossRefGoogle Scholar
Greenwood, J, Warren, P and Rubin, AE (2000) Late-stage crystallization features of Los Angeles, a new basaltic shergottite. Lunar and Planetary Science Conference, 2074.Google Scholar
Guangyin, Z and Youcai, Z (2017) Harvest of bioenergy from sewage sludge by anaerobic digestion. In Guangyin, Z and Youcai, Z (eds). Pollution Control and Resource Recovery for Sewage Sludge. Chapter 5. Butterworth-Heinemann, pp. 181–273.CrossRefGoogle Scholar
Gupta, A, Dutta, A, Sarkar, J, Panigrahi, MK and Sar, P (2018) Low-abundance members of the Firmicutes facilitate bioremediation of soil impacted by highly acidic mine drainage from the Malanjkhand copper project, India. Frontiers in Microbiology 9, 2882.CrossRefGoogle ScholarPubMed
Haberle, R, Mckay, C, Schaeffer, J, Joshi, M, Cabrol, N and Grin, E (2000) Meteorological control on the formation of Martian paleolakes.Google Scholar
Hong, Z, Chen, W, Rong, X, Cai, P, Dai, K and Huang, Q (2013) The effect of extracellular polymeric substances on the adhesion of bacteria to clay minerals and goethite. Chemical Geology 360, 118–125.CrossRefGoogle Scholar
Hutchens, E (2009) Microbial selectivity on mineral surfaces: possible implications for weathering processes. Fungal Biology Reviews 23, 115–121.CrossRefGoogle Scholar
Jakosky, B (1996) Warm havens for life on Mars. New Scientist 2028, 38–42.Google Scholar
Jakosky, BM (1998) The Search for Life on Other Planets. Cambridge University Press, pp. 336.Google Scholar
Juniper, SK, Martineu, P, Sarrazin, J and Gelinas, Y (1995) Microbial-mineral floc associated with nascent hydrothermal activity on CoAxial Segment, Juan de Fuca Ridge. Geophysical Research Letters 22, 179–182.CrossRefGoogle Scholar
Kappler, A and Newman, DK (2004) Formation of Fe(III)-minerals by Fe(II)-oxidizing photoautotrophic bacteria. Geochimica et Cosmochimica Acta 68, 1217–1226.CrossRefGoogle Scholar
Kolo, K, Konhauser, K, Krumbein, WE, Ingelgem, YV, Hubin, A and Claeys, P (2009) Microbial dissolution of hematite and associated cellular fossilization by reduced iron phases: a study of ancient microbe-mineral surface interactions. Astrobiology 9, 777–796.CrossRefGoogle ScholarPubMed
Konhauser, KO, Hamade, T, Raiswell, R, Morris, RC, Ferris, FG, Southam, G and Canfield, DE (2002) Could bacteria have formed the Precambrian banded iron formations? Geology 30, 1079–1082.2.0.CO;2>CrossRefGoogle Scholar
Kostka, JE and Nealson, KH (1995) Dissolution and reduction of magnetite by bacteria. Environmental Science & Technology 29, 2535–2540.CrossRefGoogle ScholarPubMed
Liu, C, Kota, S, Zachara, JM, Fredrickson, JK and Brinkman, CK (2001) Kinetic analysis of the bacterial reduction of goethite. Environmental Science & Technology 35, 2482–2490.CrossRefGoogle ScholarPubMed
Lovley, DR (1997) Microbial Fe(III) reduction in subsurface environments. FEMS Microbiology Reviews 20, 305–313.CrossRefGoogle Scholar
Lovley, DR, Phillips, EJ and Lonergan, DJ (1991) Enzymic versus nonenzymic mechanisms for iron(III) reduction in aquatic sediments. Environmental Science & Technology 25, 1062–1067.CrossRefGoogle Scholar
Lovley, DR, Giovannoni, SJ, White, DC, Champine, JE, Phillips, E, Gorby, YA and Goodwin, S (1993) Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Archives of Microbiology 159, 336–344.CrossRefGoogle ScholarPubMed
Lovley, DR, Holmes, DE and Nevin, KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Advances in Microbial Physiology 49, 219–286.CrossRefGoogle ScholarPubMed
Mccollom, TM (2006) The habitability of Mars: past and present. Solar System Update. Berlin, Heidelberg: Springer.Google Scholar
Mckay, CP and Stoker, CR (1989) The early environment and its evolution on Mars: implication for life. Reviews of Geophysics 27, 189–214.CrossRefGoogle Scholar
Meng, L, Zuo, R, Wang, J-S, Li, Q, Du, C, Liu, X and Chen, M (2020) Response of the redox species and indigenous microbial community to seasonal groundwater fluctuation from a typical riverbank filtration site in northeast China. Ecological Engineering, 10699.Google Scholar
Morgan, JJ and Stumm, W (1996) Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters. Vol.126. John Wiley & Sons.Google Scholar
Morris, RV, Agresti, DG, Lauer, HV JR, Newcomb, JA, Shelfer, TD and Murali, A (1989) Evidence for pigmentary hematite on Mars based on optical, magnetic, and Mossbauer studies of superparamagnetic (nanocrystalline) hematite. Journal of Geophysical Research: Solid Earth 94, 2760–2778.CrossRefGoogle Scholar
Nealson, KH (1997) The limits of life on earth and searching for life on Mars. Journal of Geophysical Research: Planets 102, 23675–23686.CrossRefGoogle ScholarPubMed
Nealson, KH and Myers, CR (1990) Iron reduction by bacteria: a potential role in the genesis of banded iron formations. American Journal of Science 290, 35–45.Google Scholar
Nealson, KH and Saffarini, D (1994) Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annual Review of Microbiology 48, 311–344.CrossRefGoogle ScholarPubMed
Ona-Nguema, G, Abdelmoula, M, Jorand, F, Benali, O, Géhin, A, Block, J-C and Génin, J-MR (2002) Iron(II, III) hydroxycarbonate green rust formation and stabilization from lepidocrocite bioreduction. Environmental Science & Technology 36, 16–20.CrossRefGoogle ScholarPubMed
Ondov, BD, Bergman, NH and Phillippy, AM (2011) Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 12, 385.CrossRefGoogle Scholar
Paul, PEV, Sangeetha, V and Deepika, RG (2019) Emerging trends in the industrial production of chemical products by microorganisms. In Buddolla, V (ed). Recent Developments in Applied Microbiology and Biochemistry. Chapter 9. Academic Press, pp. 107–125.CrossRefGoogle Scholar
Pérez-Guzmán, L, Bogner, K and Lower, B (2010) Earth's ferrous wheel. Nature Education Knowledge 3, 32.Google Scholar
Planavsky, N, Bekker, A, Rouxel, OJ, Kamber, B, Hofmann, A, Knudsen, A and Lyons, TW (2010) Rare earth element and yttrium compositions of Archean and Paleoproterozoic Fe formations revisited: new perspectives on the significance and mechanisms of deposition. Geochimica et Cosmochimica Acta 74, 6387–6405.CrossRefGoogle Scholar
Ransom, B, Bennett, RH, Baerwald, R, Hulbert, MH and Burkett, P-J (1999) In situ conditions and interactions between microbes and minerals in fine-grained marine sediments: a TEM microfabric perspective. American Mineralogist 84, 183–192.CrossRefGoogle Scholar
Rieder, R, Economou, T, Wänke, H, Turkevich, A, Crisp, J, Brückner, J, Dreibus, G and Mcsween, H (1997a) The chemical composition of Martian soil and rocks returned by the mobile alpha proton X-ray spectrometer: preliminary results from the X-ray mode. Science (New York, N.Y.) 278, 1771–1774.CrossRefGoogle Scholar
Rieder, R, Wänke, H, Economou, T and Turkevich, A (1997b) Determination of the chemical composition of Martian soil and rocks: the alpha proton X ray spectrometer. Journal of Geophysical Research: Planets 102, 4027–4044.CrossRefGoogle Scholar
Roden, EE (2006) Geochemical and microbiological controls on dissimilatory iron reduction. Comptes Rendus Geoscience 338, 456–467.CrossRefGoogle Scholar
Rogers, JR and Bennett, PC (2004) Mineral stimulation of subsurface microorganisms: release of limiting nutrients from silicates. Chemical Geology 203, 91–108.CrossRefGoogle Scholar
Roh, Y and Moon, H-S (2001) Iron reduction by a psychrotolerant Fe(III)-reducing bacterium isolated from ocean sediment. Geosciences Journal 5, 183–190.CrossRefGoogle Scholar
Röling, WF, Aerts, JW, Patty, CL, Ten Kate, IL, Ehrenfreund, P and Direito, SO (2015) The significance of microbe-mineral-biomarker interactions in the detection of life on Mars and beyond. Astrobiology 15, 492–507.CrossRefGoogle ScholarPubMed
Schwertmann, U, Taylor, R, Dixon, J and Weed, S (1989) Minerals in soil environments. In Dixon, JB and Weed, SB (eds), Soil Science Society of America Book Series. Madison, Wisconsin: EUA, p. 379.Google Scholar
Shekhtman, L (2019) With Mars Methane Mystery Unsolved, Curiosity Serves Scientists a New One: Oxygen [Online]. National Aeronautics and Space Administration. Available at https://www.nasa.gov/feature/goddard/2019/with-mars-methane-mystery-unsolved-curiosity-serves-scientists-a-new-one-oxygen (Accessed 12.12.2020 2020).Google Scholar
Soina, V, Vorobiova, E, Zvyagintsev, D and Gilichinsky, D (1995) Preservation of cell structures in permafrost: a model for exobiology. Advances in Space Research 15, 237–242.CrossRefGoogle Scholar
Trainer, MG, Wong, MH, Mcconnochie, TH, Franz, HB, Atreya, SK, Conrad, PG, Lefèvre, F, Mahaffy, PR, Malespin, CA and Manning, HL (2019) Seasonal variations in atmospheric composition as measured in Gale crater, Mars. Journal of Geophysical Research: Planets 124, 3000–3024.Google Scholar
Uroz, S, Calvaruso, C, Turpault, M-P and Frey-Klett, P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends in microbiology 17, 378–387.CrossRefGoogle ScholarPubMed
Wang, H, Hu, C, Hu, X, Yang, M and Qu, J (2012) Effects of disinfectant and biofilm on the corrosion of cast iron pipes in a reclaimed water distribution system. Water Research 46, 1070–1078.CrossRefGoogle Scholar
Weber, KA, Achenbach, LA and Coates, JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nature Reviews Microbiology 4, 752–764.CrossRefGoogle ScholarPubMed
Westall, F, Steele, A, Toporski, J, Walsh, M, Allen, C, Guidry, S, Mckay, D, Gibson, E and Chafetz, H (2000) Polymeric substances and biofilms as biomarkers in terrestrial materials: implications for extraterrestrial samples. Journal of Geophysical Research: Planets 105, 24511–24527.CrossRefGoogle Scholar
Widdel, F, Schnell, S, Heising, S, Ehrenreich, A, Assmus, B and Schink, B (1993) Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362, 834–836.CrossRefGoogle Scholar
Williams, RJP. (1989) The Functional Form of Biominerals. In Mann, S, Webb, J and Williams, RJP (eds). Biomineralization. Weinheim: VCH, pp. 1–34.Google Scholar
Wu, Y, Cai, P, Jing, X, Niu, X, Ji, D, Ashry, NM, Gao, C and Huang, Q (2019) Soil biofilm formation enhances microbial community diversity and metabolic activity. Environment International 132, 105116.CrossRefGoogle ScholarPubMed
Yin, X, Weitzel, F, Jiménez-López, CN, Griesshaber, E, Fernández-Díaz, L, Rodríguez-Navarro, A, Ziegler, A and Schmahl, WW (2020) Directing effect of bacterial extracellular polymeric substances (EPS) on calcite organization and EPS–carbonate composite Aggregate formation. Crystal Growth & Design 20, 1467–1484.CrossRefGoogle Scholar
Zachara, JM, Kukkadapu, RK, Fredrickson, JK, Gorby, YA and Smith, SC (2002) Biomineralization of poorly crystalline Fe(III) oxides by dissimilatory metal reducing bacteria (DMRB). Geomicrobiology Journal 19, 179–207.CrossRefGoogle Scholar
Zhang, G, Dong, H, Jiang, H, Kukkadapu, RK, Kim, J, Eberl, D and Xu, Z (2009) Biomineralization associated with microbial reduction of Fe3+ and oxidation of Fe2+ in solid minerals. American Mineralogist 94, 1049–1058.CrossRefGoogle Scholar
Zhang, L, Zeng, Q, Liu, X, Chen, P, Guo, X, Ma, LZ, Dong, H and Huang, Y (2019) Iron reduction by diverse Actinobacteria under oxic and pH-neutral conditions and the formation of secondary minerals. Chemical Geology 525, 390–399.CrossRefGoogle Scholar
Zhu, J, Li, Q, Jiao, W, Jiang, H, Sand, W, Xia, J, Liu, X, Qin, W, Qiu, G and Hu, Y (2012) Adhesion forces between cells of Acidithiobacillus ferrooxidans, Acidithiobacillus thiooxidans or Leptospirillum ferrooxidans and chalcopyrite. Colloids and Surfaces B: Biointerfaces 94, 95–100.CrossRefGoogle ScholarPubMed
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