Mass collection of magnetotactic bacteria from the permanently stratified ferruginous Lake Pavin, France.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
revised:
04
03
2021
received:
11
12
2020
accepted:
07
03
2021
pubmed:
10
3
2021
medline:
18
3
2022
entrez:
9
3
2021
Statut:
ppublish
Résumé
Obtaining high biomass yields of specific microorganisms for culture-independent approaches is a challenge faced by scientists studying organism's recalcitrant to laboratory conditions and culture. This difficulty is highly decreased when studying magnetotactic bacteria (MTB) since their unique behaviour allows their enrichment and purification from other microorganisms present in aquatic environments. Here, we use Lake Pavin, a permanently stratified lake in the French Massif Central, as a natural laboratory to optimize collection and concentration of MTB that thrive in the water column and sediments. A method is presented to separate MTB from highly abundant abiotic magnetic particles in the sediment of this crater lake. For the water column, different sampling approaches are compared such as in situ collection using a Niskin bottle and online pumping. By monitoring several physicochemical parameters of the water column, we identify the ecological niche where MTB live. Then, by focusing our sampling at the peak of MTB abundance, we show that the online pumping system is the most efficient for fast recovering of large volumes of water at a high spatial resolution, which is necessary considering the sharp physicochemical gradients observed in the water column. Taking advantage of aerotactic and magnetic MTB properties, we present an efficient method for MTB concentration from large volumes of water. Our methodology represents a first step for further multidisciplinary investigations of the diversity, metagenomic and ecology of MTB populations in Lake Pavin and elsewhere, as well as chemical and isotopic analyses of their magnetosomes.
Identifiants
pubmed: 33687779
doi: 10.1111/1462-2920.15458
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
721-736Informations de copyright
© 2021 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Abreu, F., Martins, J.L., Silveira, T.S., Keim, C.N., de Barros, H.G.P.L., Filho, F.J.G., and Lins, U. (2007) “Candidatus Magnetoglobus multicellularis”, a multicellular, magnetotactic prokaryote from a hypersaline environment. Int J Syst Evol Microbiol 57: 1318-1322.
Aeschbach-Hertig, W., Hofer, M., Kipfer, R., Imboden, D.M., and Wieler, R. (1999) Accumulation of mantle gases in a permanently stratified volcanic lake (Lac Pavin, France). Geochim Cosmochim Acta 63: 3357-3372.
Aeschbach-Hertig, W., Hofer, M., Schmid, M., Kipfer, R., and Imboden, D.M. (2002) The physical structure and dynamics of a deep, meromictic crater lake (Lac Pavin, France). Hydrobiologia 487: 111-136.
Albéric, P., Voillier, E., Jézéquel, D., Grosbois, C., and Michard, G. (2000) Interactions between trace elements and dissolved organic matter in the stagnant anoxic deep layer of a meromictic lake. Limnol Oceanogr 45: 1088-1096.
Amor, M., Busigny, V., Louvat, P., Gélabert, A., Cartigny, P., Durand-Dubief, M., et al. (2016) Mass-dependent and -independent signature of Fe isotopes in magnetotactic bacteria. Science 352: 705-708.
Amor, M., Busigny, V., Louvat, P., Tharaud, M., Gelabert, A., Cartigny, P., et al. (2018) Iron uptake and magnetite biomineralization in the magnetotactic bacterium Magnetospirillum magneticum strain AMB-1: an iron isotope study. Geochim Cosmochim Acta 232: 225-243.
Assayag, N., Jézéquel, D., Ader, M., Viollier, E., Michard, G., Prévot, F., and Agrinier, P. (2008) Hydrological budget, carbon sources and biogeochemical processes in Lac Pavin (France): constraints from δ18O of water and δ13C of dissolved inorganic carbon. Appl Geochem 23: 2800-2816.
Bazylinski, D.A., and Frankel, R.B. (2004) Magnetosome formation in prokaryotes. Nat Rev Microbiol 2: 217-230.
Bazylinski, D.A., Williams, T.J., Lefèvre, C.T., Berg, R.J., Zhang, C.L., Bowser, S.S., et al. (2013) Magnetococcus marinus gen. nov., sp. nov., a marine, magnetotactic bacterium that represents a novel lineage (Magnetococcaceae fam. nov.; Magnetococcales ord. nov.) at the base of the Alphaproteobacteria. Int J Syst Evol Microbiol 63: 801-808.
Berg, J.S., Jezequel, D., Duverger, A., Lamy, D., Laberty-Robert, C., and Miot, J. (2019) Microbial diversity involved in iron and cryptic sulfur cycling in the ferruginous, low-sulfate waters of Lake Pavin. PLoS One 14: e0212787.
Blainey, P.C. (2013) The future is now: single-cell genomics of bacteria and archaea. FEMS Microbiol Rev 37: 407-427.
Blakemore, R. (1975) Magnetotactic bacteria. Science 190: 377-379.
Bonhomme, C. (2008) Turbulences et ondes en milieu naturel stratifié: deux études de cas: étude du mélange turbulent et des ondes internes du lac Pavin (Auvergne, France); influence des ondes de Rossby sur la concentration en chlorophylle de surface dans l'upwelling du Pérou.
Bonhomme, C., Poulin, M., Vincon-Leite, B., Saad, M., Groleau, A., Jezequel, D., and Tassin, B. (2011) Maintaining meromixis in Lake Pavin (Auvergne, France): the key role of a sublacustrine spring. C R Geosci 343: 749-759.
Bura-Nakic, E., Viollier, E., Jezequel, D., Thiam, A., and Ciglenecki, I. (2009) Reduced sulfur and iron species in anoxic water column of meromictic crater Lake Pavin (Massif Central, France). Chem Geol 266: 311-317.
Busigny, V., Jézéquel, D., Cosmidis, J., Viollier, E., Benzerara, K., Planavsky, N.J., et al. (2016) The iron wheel in Lac Pavin: interaction with phosphorus cycle. In Lake Pavin: History, Geology, Biogeochemistry, and Sedimentology of a Deep Meromictic Maar Lake, Sime-Ngando, T., Boivin, P., Chapron, E., Jezequel, D., and Meybeck, M. (eds). Cham: Springer International Publishing, pp. 205-220.
Busigny, V., Planavsky, N.J., Jézéquel, D., Crowe, S., Louvat, P., Moureau, J., et al. (2014) Iron isotopes in an Archean Ocean analogue. Geochim Cosmochim Acta 133: 443-462.
Chapron, E., Alberic, P., Jezequel, D., Versteeg, W., Bourdier, J.-L., and Sitbon, J. (2010) Multidisciplinary characterisation of sedimentary processes in a recent maar Lake (Lake Pavin, French Massif Central) and implication for natural hazards. Nat Hazards Earth Syst Sci 10: 1815-1827.
Cosmidis, J., Benzerara, K., Morin, G., Busigny, V., Lebeau, O., Jezequel, D., et al. (2014) Biomineralization of iron-phosphates in the water column of Lake Pavin (Massif Central, France). Geochim Cosmochim Acta 126: 78-96.
Descamps, E.C.T., Monteil, C.L., Menguy, N., Ginet, N., Pignol, D., Bazylinski, D.A., and Lefèvre, C.T. (2017) Desulfamplus magnetovallimortis gen. nov., sp. nov., a magnetotactic bacterium from a brackish desert spring able to biomineralize greigite and magnetite, that represents a novel lineage in the Desulfobacteraceae. Syst Appl Microbiol 40: 280-289.
Flies, C.B., Jonkers, H.M., de Beer, D., Bosselmann, K., Bottcher, M.E., and Schüler, D. (2005) Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiol Ecol 52: 185-195.
Frankel, R.B., Bazylinski, D.A., Johnson, M.S., and Taylor, B.L. (1997) Magneto-aerotaxis in marine coccoid bacteria. Biophys J 73: 994-1000.
Jogler, C., Kube, M., Schübbe, S., Ullrich, S., Teeling, H., Bazylinski, D.A., et al. (2009a) Comparative analysis of magnetosome gene clusters in magnetotactic bacteria provides further evidence for horizontal gene transfer. Environ Microbiol 11: 1267-1277.
Jogler, C., Lin, W., Meyerdierks, A., Kube, M., Katzmann, E., Flies, C., et al. (2009b) Toward cloning of the magnetotactic metagenome: identification of magnetosome Island gene clusters in uncultivated magnetotactic bacteria from different aquatic sediments. Appl Environ Microbiol 75: 3972-3979.
Jogler, C., Niebler, M., Lin, W., Kube, M., Wanner, G., Kolinko, S., et al. (2010) Cultivation-independent characterization of “Candidatus Magnetobacterium bavaricum” via ultrastructural, geochemical, ecological and metagenomic methods. Environ Microbiol 12: 2466-2478.
Jogler, C., and Schüler, D. (2009) Genomics, genetics, and cell biology of magnetosome formation. Annu Rev Microbiol 63: 501-521.
Kolinko, S., Richter, M., Glöckner, F.-O., Brachmann, A., and Schüler, D. (2016) Single-cell genomics of uncultivated deep-branching magnetotactic bacteria reveals a conserved set of magnetosome genes. Environ Microbiol 18: 21-37.
Kolinko, S., Wanner, G., Katzmann, E., Kiemer, F., Fuchs, B.M., and Schüler, D. (2013) Clone libraries and single cell genome amplification reveal extended diversity of uncultivated magnetotactic bacteria from marine and freshwater environments. Environ Microbiol 15: 1290-1301.
Koziaeva, V.V., Alekseeva, L.M., Uzun, M.M., Leão, P., Sukhacheva, M.V., Patutina, E.O., et al. (2020) Biodiversity of magnetotactic bacteria in the freshwater Lake Beloe Bordukovskoe, Russia. Microbiology 89: 348-358.
Lefèvre, C.T. (2016) Genomic insights into the early-diverging magnetotactic bacteria. Environ Microbiol 18: 1-3.
Lefèvre, C.T., and Bazylinski, D.A. (2013) Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol Mol Biol Rev 77: 497-526.
Lefèvre, C.T., Bennet, M., Landau, L., Vach, P., Pignol, D., Bazylinski, D.A., et al. (2014) Diversity of magneto-aerotactic behaviors and oxygen sensing mechanisms in cultured magnetotactic bacteria. Biophys J 107: 527-538.
Lefèvre, C.T., Bernadac, A., Yu-Zhang, K., Pradel, N., and Wu, L.-F. (2009) Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. Environ Microbiol 11: 1646-1657.
Lefèvre, C.T., Frankel, R.B., Abreu, F., Lins, U., and Bazylinski, D.A. (2011) Culture-independent characterization of a novel, uncultivated magnetotactic member of the Nitrospirae phylum. Environ Microbiol 13: 538-549.
Lefèvre, C.T., Howse, P.A., Schmidt, M.L., Sabaty, M., Menguy, N., Luther, G.W., and Bazylinski, D.A. (2016) Growth of magnetotactic sulfate-reducing bacteria in oxygen concentration gradient medium. Environ Microbiol Rep 8: 1003-1015.
Lefèvre, C.T., Schmidt, M.L., Viloria, N., Trubitsyn, D., Schüler, D., and Bazylinski, D.A. (2012) Insight into the evolution of magnetotaxis in Magnetospirillum spp., based on mam gene phylogeny. Appl Environ Microbiol 78: 7238-7248.
Li, J., Ge, X., Zhang, X., Chen, G., and Pan, Y. (2010) Recover vigorous cells of Magnetospirillum magneticum AMB-1 by capillary magnetic separation. Chin J Ocean Limnol 28: 826-831.
Li, J., Liu, P., Wang, J., Roberts, A.P., and Pan, Y. (2020c) Magnetotaxis as an adaptation to enable bacterial shuttling of microbial sulfur and sulfur cycling across aquatic oxic-anoxic interfaces. J Geophys Res-Biogeosci 125: e2020JG006012.
Li, J., Menguy, N., Gatel, C., Boureau, V., Snoeck, E., Patriarche, G., et al. (2015) Crystal growth of bullet-shaped magnetite in magnetotactic bacteria of the Nitrospirae phylum. J R Soc Interface 12: 20141288.
Li, J., Menguy, N., Leroy, E., Roberts, A.P., Liu, P., and Pan, Y. (2020a) Biomineralization and magnetism of uncultured Magnetotactic coccus strain THC-1 with non-chained magnetosomal magnetite nanoparticles. J Geophys Res Solid Earth 125: e2020JB020853.
Li, J., Menguy, N., Roberts, A.P., Gu, L., Leroy, E., Bourgon, J., et al. (2020b) Bullet-shaped magnetite biomineralization within a magnetotactic deltaproteobacterium: implications for magnetofossil identification. J Geophys Res Biogeosc 125: e2020JG005680.
Li, J., Zhang, H., Liu, P., Menguy, N., Roberts, A.P., Chen, H., et al. (2019) Phylogenetic and structural identification of a novel magnetotactic deltaproteobacteria strain, WYHR-1, from a freshwater lake. Appl Environ Microbiol 85: e00731-19.
Li, J., Zhang, H., Menguy, N., Benzerara, K., Wang, F., Lin, X., et al. (2017) Single-cell resolution of uncultured magnetotactic bacteria via fluorescence-coupled electron microscopy. Appl Environ Microbiol 83: pii: e00409-17.
Lin, W., Li, J., and Pan, Y. (2012) Newly isolated but uncultivated magnetotactic bacterium of the phylum Nitrospirae from Beijing, China. Appl Environ Microbiol 78: 668-675.
Lin, W., Pan, Y., and Bazylinski, D.A. (2017) Diversity and ecology of and biomineralization by magnetotactic bacteria. Environ Microbiol Rep 9: 345-356.
Lin, W., Tian, L., Li, J., and Pan, Y. (2008) Does capillary racetrack-based enrichment reflect the diversity of uncultivated magnetotactic cocci in environmental samples? FEMS Microbiol Lett 279: 202-206.
Lin, W., Wang, Y., Gorby, Y., Nealson, K., and Pan, Y. (2013) Integrating niche-based process and spatial process in biogeography of magnetotactic bacteria. Sci Rep 3: 1643.
Lin, W., Zhang, W., Zhao, X., Roberts, A.P., Paterson, G.A., Bazylinski, D.A., and Pan, Y. (2018) Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with lineage-specific evolution. ISME J 12: 1508-1519.
Lins, U., Freitas, F., Keim, C.N., de Barros, H.L., Esquivel, D.M.S., and Farina, M. (2003) Simple homemade apparatus for harvesting uncultured magnetotactic microorganisms. Braz J Microbiol 34: 111-116.
Liu, J., Zhang, W., Du, H., Leng, X., Li, J.-H., Pan, H., et al. (2018) Seasonal changes in the vertical distribution of two types of multicellular magnetotactic prokaryotes in the sediment of Lake Yuehu, China. Environ Microbiol Rep 10: 475-484.
Liu, P., Liu, Y., Zhao, X., Roberts, A.P., Zhang, H., Zheng, Y., et al. (2020) Diverse phylogeny and morphology of magnetite biomineralized by magnetotactic cocci. Environ Microbiol 23, 1115-1129.
Lopes, F., Viollier, E., Thiam, A., Michard, G., Abril, G., Groleau, A., et al. (2011) Biogeochemical modelling of anaerobic vs. aerobic methane oxidation in a meromictic crater lake (Lake Pavin, France). Appl Geochem 26: 1919-1932.
Michard, G., Viollier, E., Jézéquel, D., and Sarazin, G. (1994) Geochemical study of a crater lake: Pavin Lake, France-identification, location and quantification of the chemical reactions in the lake. Chem Geol 115: 103-115.
Miot, J., Jezequel, D., Benzerara, K., Cordier, L., Rivas-Lamelo, S., Skouri-Panet, F., et al. (2016) Mineralogical diversity in Lake Pavin: connections with water column chemistry and biomineralizmmmation processes. Minerals 6: 24.
Monteil, C.L., Benzerara, K., Menguy, N., Bidaud, C.C., Michot-Achdjian, E., Bolzoni, R., et al. (2021) Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria. ISME J 15: 1-18.
Monteil, C.L. and Lefevre, C.T. (2019) Magnetoreception in microorganisms. Trends Microbiol 28: 266-275.
Monteil, C.L., Vallenet, D., Menguy, N., Benzerara, K., Barbe, V., Fouteau, S., et al. (2019) Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist. Nat Microbiol 4: 1088-1095.
Moskowitz, B.M., Bazylinski, D.A., Egli, R., Frankel, R.B., and Edwards, K.J. (2008) Magnetic properties of marine magnetotactic bacteria in a seasonally stratified coastal pond (Salt Pond, MA, USA). Geophys J Int 174: 75-92.
Oestreicher, Z., Lower, S., and Lower, B. (2011) Magnetotactic bacteria containing phosphorus-rich inclusion bodies. Microsc Microanal 17: 140-141.
Pan, H., Dong, Y., Teng, Z., Li, J., Zhang, W., Xiao, T., and Wu, L.-F. (2019) A species of magnetotactic deltaproteobacterium was detected at the highest abundance during an algal bloom. FEMS Microbiol Lett: 366:fnz253.
Popp, F., Armitage, J.P., and Schüler, D. (2014) Polarity of bacterial magnetotaxis is controlled by aerotaxis through a common sensory pathway. Nat Commun 5: 5398.
Qian, X.-X., Santini, C.-L., Kosta, A., Menguy, N., Le Guenno, H., Zhang, W., et al. (2020) Juxtaposed membranes underpin cellular adhesion and display unilateral cell division of multicellular magnetotactic prokaryotes. Environ Microbiol 22: 1481-1494.
R Core Team. (2018) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/.
Rivas-Lamelo, S., Benzerara, K., Lefèvre, C.T., Jézéquel, D., Menguy, N., Viollier, E., et al. (2017) Magnetotactic bacteria as a new model for P sequestration in the ferruginous Lake Pavin. Geochem Perspect Lett 5: 35-41.
Schettler, G., Schwab, M.J., and Stebich, M. (2007) A 700-year record of climate change based on geochemical and palynological data from varved sediments (Lac Pavin, France). Chem Geol 240: 11-35.
Schüler, D. (2002) The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. Int Microbiol 5: 209-214.
Schulz-Vogt, H.N., Pollehne, F., Jürgens, K., Arz, H.W., Beier, S., Bahlo, R., et al. (2019) Effect of large magnetotactic bacteria with polyphosphate inclusions on the phosphate profile of the suboxic zone in the Black Sea. ISME J 13: 1198-1208.
Simmons, S.L., Bazylinski, D.A., and Edwards, K.J. (2007) Population dynamics of marine magnetotactic bacteria in a meromictic salt pond described with qPCR. Environ Microbiol 9: 2162-2174.
Simmons, S.L., Sievert, S.M., Frankel, R.B., Bazylinski, D.A., and Edwards, K.J. (2004) Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Appl Environ Microbiol 70: 6230-6239.
Spring, S., Amann, R., Ludwig, W., Schleifer, K.H., Schuler, D., Poralla, K., and Petersen, N. (1994) Phylogenetic analysis of uncultured magnetotactic bacteria from the alpha-subclass of Proteobacteria. Syst Appl Microbiol 17: 501-508.
Spring, S., Amann, R., Ludwig, W., Schleifer, K.H., Vangemerden, H., and Petersen, N. (1993) Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a fresh-water sediment. Appl Environ Microbiol 59: 2397-2403.
Viollier, E., Jezequel, D., Michard, G., Pepe, M., Sarazin, G., and Alberic, P. (1995) Geochemical study of a Crater Lake (Pavin Lake, France)-trace-element behavior in the monimolimnion. Chem Geol 125: 61-72.
Wolfe, R.S., Thauer, R.K., and Pfennig, N. (1987) A ‘capillary racetrack’ method for isolation of magnetotactic bacteria. FEMS Microbiol Lett 45: 31-35.
Xiao, Z., Lian, B., Chen, J., and Teng, H.H. (2007) Design and application of the method for isolating magnetotactic bacteria. Chin J Geochem 26: 252-258.
Zhang, H., Menguy, N., Wang, F., Benzerara, K., Leroy, E., Liu, P., et al. (2017) Magnetotactic coccus strain SHHC-1 affiliated to Alphaproteobacteria forms octahedral magnetite magnetosomes. Front Microbiol 8: 969.