Articles | Volume 19, issue 18
https://doi.org/10.5194/bg-19-4533-2022
© Author(s) 2022. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/bg-19-4533-2022
© Author(s) 2022. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
| 
21 Sep 2022
Research article |
| 21 Sep 2022
| 21 Sep 2022
Do bacterial viruses affect framboid-like mineral formation?
Faculty of Geology, Geophysics and Environmental Protection, AGH University of Science and Technology, Al. Mickiewicza 30, 30-059 Kraków, Poland
Marcin D. Syczewski
Faculty of Geology, University of Warsaw, ul. Żwirki i Wigury 93, 02-089 Warsaw, Poland
Kamil Kornaus
Faculty of Materials Science and Ceramics, AGH University of Science and Technology, Al. Mickiewicza 30, 30-059 Kraków, Poland
Mirosław Słowakiewicz
Faculty of Geology, University of Warsaw, ul. Żwirki i Wigury 93, 02-089 Warsaw, Poland
Łukasz Zych
Faculty of Materials Science and Ceramics, AGH University of Science and Technology, Al. Mickiewicza 30, 30-059 Kraków, Poland
Andrzej Borkowski
Faculty of Geology, Geophysics and Environmental Protection, AGH University of Science and Technology, Al. Mickiewicza 30, 30-059 Kraków, Poland
Related authors
No articles found.
Izabela De Mey-Śnieżyńska, Mirosław Słowakiewicz, Francien Peterse, Aleksandra Brodecka-Goluch, Andrzej Borkowski, and Katarzyna Łukawska-Matuszewska
EGUsphere, https://doi.org/10.5194/egusphere-2026-519, https://doi.org/10.5194/egusphere-2026-519, 2026
This preprint is open for discussion and under review for Biogeosciences (BG).
Short summary
Short summary
This study examined seafloor fluid-venting craters (‘pockmarks’) to understand what drives the microbes inhabiting this environment. By combining lipid biomarkers extracted from seabed sediments with genetic analyses, it was found that microbial community composition is shaped mainly by groundwater inflow, nitrogen availability, and methane seepage. Pockmarks may therefore modulate coastal nutrient cycling and greenhouse gas dynamics, which is relevant for ecosystem monitoring.
Cited articles
Aishwarya, S., Gunasekaran, K., Kumar, P. S., Begum, A., Shantha, E., Jeevitha, V., and Gayathri, K. V.:
Structural, functional, resistome and pathogenicity profiling of the Cooum river, Microb. Pathogenesis, 158, 105048, https://doi.org/10.1016/j.micpath.2021.105048, 2021.
Bellas, C. M. and Anesio, A. M.:
High diversity and potential origins of T4-type bacteriophages on the surface of Arctic glaciers, Extremophiles, 17, 861–870, https://doi.org/10.1007/s00792-013-0569-x, 2013.
Berner, R. A.:
The synthesis of framboidal pyrite, Econ. Geol., 64, 383–384, https://doi.org/10.2113/gsecongeo.64.4.383, 1969.
Butler, I. B. and Rickard, D.:
Framboidal pyrite formation via the oxidation of iron(II) monosulfide by hydrogen sulphide, Geochim. Cosmochim. Ac., 64, 2665–2672, https://doi.org/10.1016/S0016-7037(00)00387-2, 2000.
Carreira, C., Piel, T., Staal, M., Stuut, J.-B. W., Middelboe, M., and Brussaard, C. P. D.:
Microscale spatial distributions of microbes and viruses in intertidal photosynthetic microbial mats, SpringerPlus, 4, 239, https://doi.org/10.1186/s40064-015-0977-8, 2015.
Chen, L., Huang, L., Méndez-García, C., Kuang, J., Hua, Z., Liu, J., and Shu, W.:
Microbial communities, processes and functions in acid mine drainage ecosystems, Curr. Opin. Biotech., 38, 150–158, https://doi.org/10.1016/j.copbio.2016.01.013, 2016.
Collins, A. M.:
Petrology of the Eocene Marquez Shale Member of the Reklaw Formation, Bastrop County, Texas, The University of Texas at Austin, https://doi.org/10.26153/tsw/1322, 1982.
Daughney, C. J., Châtellier, X., Chan, A., Kenward, P., Fortin, D., Suttle, C. A., and Fowle, D. A.:
Adsorption and precipitation of iron from seawater on a marine bacteriophage (PWH3A-P1), Mar. Chem., 91, 101–115, https://doi.org/10.1016/j.marchem.2004.06.003, 2004.
Day, L. A. and Wiseman, R. L.:
A Comparison of DNA Packaging in the Virions of fd, Xf, and Pf1, Cold Spring Harbor M., 8, 605–625, 1978.
De Wit, R., Gautret, P., Bettarel, Y., Roques, C., Marlière, C., Ramonda, M., Nguyen Thanh, T., Tran Quang, H., and Bouvier, T.:
Viruses Occur Incorporated in Biogenic High-Mg Calcite from Hypersaline Microbial Mats, PLOS ONE, 10, e0130552, https://doi.org/10.1371/journal.pone.0130552, 2015.
Derjaguin, B. and Landau, L.:
Theory of the stability of strongly charged lyophobic sols and of the adhesion of strongly charged particles in solutions of electrolytes, Prog. Surf. Sci., 43, 30–59, https://doi.org/10.1016/0079-6816(93)90013-L, 1993.
Donald, R. and Southam, G.:
Low temperature anaerobic bacterial diagenesis of ferrous monosulfide to pyrite, Geochim. Cosmochim. Ac., 63, 2019–2023, https://doi.org/10.1016/S0016-7037(99)00140-4, 1999.
Działak, P., Syczewski, M., Kornaus, K., Słowakiewicz, M., Zych, L., and Borkowski, A.: Do bacterial viruses affect framboid-like mineral formation?, Zenodo [data set], https://doi.org/10.5281/zenodo.7070164, 2022.
Farrand, M.:
Framboidal sulphides precipitated synthetically, Miner. Deposita, 5, 237–247, https://doi.org/10.1007/BF00201990, 1970.
Fermin, G., Mazumdar-Leighton, S., and Tennant, P.:
Viruses of Prokaryotes, Protozoa, Fungi, and Chromista, in: Viruses, Academic Press, London, 217–244, https://doi.org/10.1016/B978-0-12-811257-1.00009-7, 2018.
Folk, R. L.:
Nannobacteria and the formation of framboidal pyrite: Textural evidence, J. Earth Syst. Sci., 114, 369–374, https://doi.org/10.1007/BF02702955, 2005.
Fuhrman, J. A.:
Marine viruses and their biogeochemical and ecological effects, Nature, 399, 541–548, https://doi.org/10.1038/21119, 1999.
Graham, U. M. and Ohmoto, H.:
Experimental study of formation mechanisms of hydrothermal pyrite, Geochim. Cosmochim. Ac., 58, 2187–2202, https://doi.org/10.1016/0016-7037(94)90004-3, 1994.
Hobbs, Z. and Abedon, S. T.:
Diversity of phage infection types and associated terminology: the problem with ‘Lytic or lysogenic’, FEMS Microbiol. Lett., 363, fnw047, https://doi.org/10.1093/femsle/fnw047, 2016.
Hua, X. and Buseck, P. R.:
Unusual forms of magnetite in the Orgueil carbonaceous chondrite, Meteorit. Planet. Sci., 33, A215–A220, https://doi.org/10.1111/j.1945-5100.1998.tb01335.x, 1998.
Ivanovska, I. L., de Pablo, P. J., Ibarra, B., Sgalari, G., MacKintosh, F. C., Carrascosa, J. L., Schmidt, C. F., and Wuite, G. J. L.:
Bacteriophage capsids: Tough nanoshells with complex elastic properties, P. Natl. Acad. Sci. USA, 101, 7600–7605, https://doi.org/10.1073/pnas.0308198101, 2004.
Kalatha, S. and Economou-Eliopoulos, M.:
Framboidal pyrite and bacterio-morphic goethite at transitional zones between Fe–Ni-laterites and limestones: Evidence from Lokris, Greece, Ore Geol. Rev., 65, 413–425, https://doi.org/10.1016/j.oregeorev.2014.10.012, 2015.
Kerridge, J. F.:
Some observations on the nature of magnetite in the Orgueil meteorite, Earth Planet. Sc. Lett., 9, 299–306, https://doi.org/10.1016/0012-821X(70)90122-6, 1970.
Kobluk, D. R. and Risk, M. J.: Algal borings and framboidal pyrite in Upper Ordovician brachiopods, Lethaia, 10, 135–143, https://doi.org/10.1111/j.1502-3931.1977.tb00602.x, 1977.
Kortenski, J. and Kostova, I.:
Occurrence and morphology of pyrite in Bulgarian coals, Int. J. Coal Geol., 29, 273–290, https://doi.org/10.1016/0166-5162(95)00033-X, 1996.
Kozina, N., Reykhard, L., Dara, O., and Gordeev, V.:
Framboidal pyrite formation in the bottom sediments of the South Caspian Basin under conditions of hydrogen sulfide contamination, Russ. J. Earth Sci., 18, 1–10, https://doi.org/10.2205/2018ES000639, 2018.
Kyle, J. E., Pedersen, K., and Ferris, F. G.:
Virus Mineralization at Low pH in the Rio Tinto, Spain, Geomicrobiol. J., 25, 338–345, https://doi.org/10.1080/01490450802402703, 2008.
Laidler, J. R. and Stedman, K. M.:
Virus Silicification under Simulated Hot Spring Conditions, Astrobiology, 10, 569–576, https://doi.org/10.1089/ast.2010.0463, 2010.
Laurinavičius, S., Käkelä, R., Bamford, D. H., and Somerharju, P.:
The origin of phospholipids of the enveloped bacteriophage phi6, Virology, 326, 182–190, https://doi.org/10.1016/j.virol.2004.05.021, 2004.
Liu, B., Wu, S., Song, Q., Zhang, X., and Xie, L.:
Two Novel Bacteriophages of Thermophilic Bacteria Isolated from Deep-Sea Hydrothermal Fields, Curr. Microbiol., 53, 163–166, https://doi.org/10.1007/s00284-005-0509-9, 2006.
Lossouarn, J., Dupont, S., Gorlas, A., Mercier, C., Bienvenu, N., Marguet, E., Forterre, P., and Geslin, C.:
An abyssal mobilome: viruses, plasmids and vesicles from deep-sea hydrothermal vents, Res. Microbiol., 166, 742–752, https://doi.org/10.1016/j.resmic.2015.04.001, 2015.
Louten, J.:
Chapter 2 – Virus Structure and Classification, in: Essential Human Virology, edited by: Louten, J., Academic Press, Boston, 19–29, https://doi.org/10.1016/B978-0-12-800947-5.00002-8, 2016.
Love, L. G. and Zimmerman, D. O.:
Bedded pyrite and micro-organisms from the Mount Isa shale, Econ. Geol., 56, 873–896, https://doi.org/10.2113/gsecongeo.56.5.873, 1961.
Lowenstam, H. A.:
Minerals Formed by Organisms, Science, 211, 1126–1131, https://doi.org/10.1126/science.7008198, 1981.
Lowenstam, H. A. and Weiner, S.:
Biomineralization Processes, in: Biomineralization Processes, Oxford University Press, New York, https://doi.org/10.1093/oso/9780195049770.003.0005, 1989.
Luther, G. W.:
Pyrite synthesis via polysulfide compounds, Geochim. Cosmochim. Ac., 55, 2839–2849, https://doi.org/10.1016/0016-7037(91)90449-F, 1991.
Mann, S.:
Molecular recognition in biomineralization, Nature, 332, 119–124, https://doi.org/10.1038/332119a0, 1988.
Merinero, R., Lunar, R., and Somoza, L. D.-D.-R.:
Nucleation, growth and oxidation of framboidal pyrite associated with hydrocarbon-derived submarine chimneys: lessons learned from the Gulf of Cadiz, Eur. J. Mineral., 21, 947–961, https://doi.org/10.1127/0935-1221/2009/0021-1956, 2009.
Millard, A. D., Pearce, D., and Zwirglmaier, K.:
Biogeography of bacteriophages at four hydrothermal vent sites in the Antarctic based on g23 sequence diversity, FEMS Microbiol. Lett., 363, fnw043, https://doi.org/10.1093/femsle/fnw043, 2016.
Murowchick, J. B. and Barnes, H. L.:
Effects of temperature and degree of supersaturation on pyrite morphology, Am. Mineral., 72, 1241–1250, 1987.
Muyzer, G. and Stams, A. J. M.:
The ecology and biotechnology of sulphate-reducing bacteria, Nat. Rev. Microbiol., 6, 441–454, https://doi.org/10.1038/nrmicro1892, 2008.
Nam, K. T., Peelle, B. R., Lee, S.-W., and Belcher, A. M.:
Genetically Driven Assembly of Nanorings Based on the M13 Virus, Nano Lett., 4, 23–27, https://doi.org/10.1021/nl0347536, 2004.
Nuhfer, E. B. and Pavlovic, A. S.:
Association of kaolinite with pyritic framboids; discussion, J. Sediment. Res., 49, 321–323, https://doi.org/10.1306/212F772F-2B24-11D7-8648000102C1865D, 1979.
Ohfuji, H. and Akai, J.:
Icosahedral domain structure of framboidal pyrite, Am. Mineral., 87, 176–180, https://doi.org/10.2138/am-2002-0119, 2002.
Ohfuji, H. and Rickard, D.:
Experimental syntheses of framboids—a review, Earth-Sci. Rev., 71, 147–170, https://doi.org/10.1016/j.earscirev.2005.02.001, 2005.
Orange, F., Chabin, A., Gorlas, A., Lucas-Staat, S., Geslin, C., Le Romancer, M., Prangishvili, D., Forterre, P., and Westall, F.:
Experimental fossilisation of viruses from extremophilic Archaea, Biogeosciences, 8, 1465–1475, https://doi.org/10.5194/bg-8-1465-2011, 2011.
Pacton, M., Wacey, D., Corinaldesi, C., Tangherlini, M., Kilburn, M. R., Gorin, G. E., Danovaro, R., and Vasconcelos, C.:
Viruses as new agents of organomineralization in the geological record, Nat. Commun., 5, 4298, https://doi.org/10.1038/ncomms5298, 2014.
Pacton, M., Sorrel, P., Bevillard, B., Zacaï, A., Vinçon-Laugier, A., and Oberhänsli, H.:
Sedimentary facies analyses from nano- to millimetre scale exploring past microbial activity in a high-altitude lake (Lake Son Kul, Central Asia), Geol. Mag., 152, 902–922, https://doi.org/10.1017/S0016756814000831, 2015.
Peng, X., Xu, H., Jones, B., Chen, S., and Zhou, H.:
Silicified virus-like nanoparticles in an extreme thermal environment: implications for the preservation of viruses in the geological record, Geobiology, 11, 6, 511–526, https://doi.org/10.1111/gbi.12052, 2013.
Pennafirme, S., Pereira, D. C., Pedrosa, L. G. M., Machado, A. S., Silva, G. O. A., Keim, C. N., Lima, I., Lopes, R. T., Paixão, I. C. N. P., and Crapez, M. A. C.:
Characterization of microbial mats and halophilic virus-like particles in a eutrophic hypersaline lagoon (Vermelha Lagoon, RJ, Brazil), Reg. Stud. Mar. Sci., 31, 100769, https://doi.org/10.1016/j.rsma.2019.100769, 2019.
Perri, E., Tucker, M. E., Słowakiewicz, M., Whitaker, F., Bowen, L., and Perrotta, I. D.:
Carbonate and silicate biomineralization in a hypersaline microbial mat (Mesaieed sabkha, Qatar): Roles of bacteria, extracellular polymeric substances and viruses, Sedimentology, 65, 1213–1245, https://doi.org/10.1111/sed.12419, 2018.
Perri, E., Słowakiewicz, M., Perrotta, I. D., and Tucker, M. E.:
Biomineralization processes in modern calcareous tufa: Possible roles of viruses, vesicles and extracellular polymeric substances (Corvino Valley – Southern Italy), Sedimentology, 69, 399–422, https://doi.org/10.1111/sed.12932, 2022.
Picard, A., Gartman, A., Clarke, D. R., and Girguis, P. R.:
Sulfate-reducing bacteria influence the nucleation and growth of mackinawite and greigite, Geochim. Cosmochim. Ac., 220, 367–384, https://doi.org/10.1016/j.gca.2017.10.006, 2018.
Popa, R., Kinkle, B. K., and Badescu, A.:
Pyrite Framboids as Biomarkers for Iron-Sulfur Systems, Geomicrobiol. J., 21, 193–206, https://doi.org/10.1080/01490450490275497, 2004.
Prestel, E., Salamitou, S., and DuBow, M. S.:
An examination of the bacteriophages and bacteria of the Namib desert, J. Microbiol., 46, 364–372, https://doi.org/10.1007/s12275-008-0007-4, 2008.
Schallreuter, R.:
Framboidal pyrite in deep-sea sediments, Initial Rep. Deep Sea Drill. Proj., 75, 875–891, 1984.
Scott, R. J., Meffre, S., Woodhead, J., Gilbert, S. E., Berry, R. F., and Emsbo, P.:
Development of Framboidal Pyrite During Diagenesis, Low-Grade Regional Metamorphism, and Hydrothermal Alteration, Econ. Geol., 104, 1143–1168, https://doi.org/10.2113/gsecongeo.104.8.1143, 2009.
Sharma, S., Chatterjee, S., Datta, S., Prasad, R., Dubey, D., Prasad, R. K., and Vairale, M. G.:
Bacteriophages and its applications: an overview, Folia Microbiol. (Praha), 62, 17–55, https://doi.org/10.1007/s12223-016-0471-x, 2017.
Skei, J. M.:
Formation of framboidal iron sulfide in the water of a permanently anoxic fjord – Framvaren, South Norway, Mar. Chem., 23, 345–352, https://doi.org/10.1016/0304-4203(88)90103-X, 1988.
Slocik, J. M., Naik, R. R., Stone, M. O., and Wright, D. W.:
Viral templates for gold nanoparticle synthesis, J. Mater. Chem., 15, 749, https://doi.org/10.1039/b413074j, 2005.
Słowakiewicz, M., Borkowski, A., Syczewski, M. D., Perrota, I. D., Owczarek, F., Sikora, A., Detman, A., Perri, E., and Tucker, M. E.:
Newly-discovered interactions between bacteriophages and the process of calcium carbonate precipitation, Geochim. Cosmochim. Ac., 292, 482–498, https://doi.org/10.1016/j.gca.2020.10.012, 2021.
Steward, G., Smith, D., and Azam, F.:
Abundance and production of bacteria and viruses in the Bering and Chukchi Seas, Mar. Ecol. Prog. Ser., 131, 287–300, https://doi.org/10.3354/meps131287, 1996.
Suttle, C. A.:
Marine viruses — major players in the global ecosystem, Nat. Rev. Microbiol., 5, 801–812, https://doi.org/10.1038/nrmicro1750, 2007.
Sweeney, R. E. and Kaplan, I. R.:
Pyrite Framboid Formation; Laboratory Synthesis and Marine Sediments, Econ. Geol., 68, 618–634, https://doi.org/10.2113/gsecongeo.68.5.618, 1973.
Taylor, G. R.:
A mechanism for framboid formation as illustrated by a volcanic exhalative sediment, Miner. Deposita, 17, 23–36, https://doi.org/10.1007/BF00206374, 1982.
Verwey, E. J. W.:
Theory of the Stability of Lyophobic Colloids, J. Phys. Chem., 51, 631–636,
https://doi.org/10.1021/j150453a001, 1947.
Vidaver, A. K., Koski, R. K., and Etfen, J. L. V.:
Bacteriophage φ6: a Lipid-Containing Virus of Pseudomonas phaseolicolal, J. Virol., 11, 799–805, https://doi.org/10.1128/JVI.11.5.799-805.1973, 1973.
Wang, Q. and Morse, J. W.:
Pyrite formation under conditions approximating those in anoxic sediments I. Pathway and morphology, Mar. Chem., 52, 99–121, https://doi.org/10.1016/0304-4203(95)00082-8, 1996.
Weitz, J. S. and Wilhelm, S. W.:
Ocean viruses and their effects on microbial communities and biogeochemical cycles, F1000 Biol. Rep., 4, 17, https://doi.org/10.3410/B4-17, 2012.
White, T. S., Morrison, J. L., and Kump, L. R.:
Formation of Iron Sulfides in Modern Salt Marsh Sediments (Wallops Island, Virginia), in: Geochemistry of Sulfur in Fossil Fuels, edited by: Editor(s): Orr, W. L. and White, C. M., vol. 429, American Chemical Society, 204–217, https://doi.org/10.1021/bk-1990-0429.ch011, 1990.
Wiese, R. G. and Fyfe, W. S.:
Occurrences of iron sulfides in Ohio coals, Int. J. Coal Geol., 6, 251–276, https://doi.org/10.1016/0166-5162(86)90004-2, 1986.
Wilkin, R., Arthur, M., and Dean, W.:
History of water-column anoxia in the Black Sea indicated by pyrite framboid size distributions, Earth Planet. Sc. Lett., 148, 517–525, https://doi.org/10.1016/S0012-821X(97)00053-8, 1997.
Wilkin, R. T. and Barnes, H. L.:
Pyrite formation by reactions of iron monosulfides with dissolved inorganic and organic sulfur species, Geochim. Cosmochim. Ac., 60, 4167–4179, https://doi.org/10.1016/S0016-7037(97)81466-4, 1996.
Wilkin, R. T. and Barnes, H. L.:
Formation processes of framboidal pyrite, Geochim. Cosmochim. Ac., 61, 323–339, https://doi.org/10.1016/S0016-7037(96)00320-1, 1997.
Wilkin, R. T., Barnes, H. L., and Brantley, S. L.:
The size distribution of framboidal pyrite in modern sediments: An indicator of redox conditions, Geochim. Cosmochim. Ac., 60, 3897–3912, https://doi.org/10.1016/0016-7037(96)00209-8, 1996.
Wittebole, X., De Roock, S., and Opal, S. M.:
A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens, Virulence, 5, 226–235, https://doi.org/10.4161/viru.25991, 2014.
Wolthers, M.:
Geochemistry and environmental mineralogy of the iron-sulphur-arsenic system: = Geochemie en milieumineralogie van het ijzer-zwavel-arseen systeem, Univ. Utrecht, ISBN: 9057440830, 185 pp., 2003.
Wolthers, M., Butler, I. B., Rickard, D., and Mason, P. R. D.:
Arsenic Uptake by Pyrite at Ambient Environmental Conditions: A Continuous-Flow Experiment, in: Advances in Arsenic Research, edited by: O'Day, P. A., Vlassopoulos, D., Meng, X., and Benning, L. G., vol. 915, American Chemical Society, 60–76, https://doi.org/10.1021/bk-2005-0915.ch005, 2005.
Short summary
Bacteriophages comprise one of the factors that may influence mineralization processes. The number of bacteriophages in the environment usually exceeds the number of bacteria by an order of magnitude. One of the more interesting processes is the formation of framboidal pyrite, and it is not entirely clear what processes determine its formation. Our studies indicate that some bacterial viruses may influence the formation of framboid-like or spherical structures.
Bacteriophages comprise one of the factors that may influence mineralization processes. The...
Altmetrics
Final-revised paper
Preprint