Cite this paper:
Haijian DU, Wenyan ZHANG, Wei LIN, Hongmiao PAN, Tian XIAO, Long-Fei WU. Genomic analysis of a pure culture of magnetotactic bacterium Terasakiella sp. SH-1[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2097-2106

Genomic analysis of a pure culture of magnetotactic bacterium Terasakiella sp. SH-1
Haijian DU1,2, Wenyan ZHANG2,3,4,7, Wei LIN5,6,7, Hongmiao PAN2,3,4,7, Tian XIAO2,3,4,7, Long-Fei WU7,8
1 College of Life Science, Shandong University, Qingdao 266237, China;
2 CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
3 Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology(Qingdao), Qingdao 266237, China;
4 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China;
5 Key Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China;
6 Institutions of Earth Science, Chinese Academy of Sciences, Beijing 100029, China;
7 France-China Joint Laboratory for Evolution and Development of Magnetotactic Multicellular Organisms, Chinese Academy of Sciences, Beijing 100029, China;
8 Aix-Marseille University, CNRS, LCB, Marseille F-13402, France
Abstract:
Magnetotactic bacteria (MTB) display magnetotaxis ability because of biomineralization of intracellular nanometer-sized, membrane-bound organelles termed magnetosomes. Despite having been discovered more than half a century, only a few representatives of MTB have been isolated and cultured in the laboratory. In this study, we report the genomic characterization of a novel marine magnetotactic spirillum strain SH-1 belonging to the genus Terasakiella that was recently isolated. A gene encoding haloalkane dehalogenase, which is involved in the degradation of chlorocyclohexane, chlorobenzene, chloroalkane, and chloroalkene, was identified. SH-1 genome contained cysCHI and soxBAZYX genes, thus potentially capable of assimilatory sulfate reduction to H2S and using thiosulfate as electron donors and oxidizing it to sulfate. Genome of SH-1 also contained genes encoding periplasmic dissimilatory nitrate reductases (napAB), assimilatory nitrate reductase (nasA) and assimilatory nitrite reductases (nasB), suggesting that it is capable of gaining energy by converting nitrate to ammonia. The pure culture of Terasakiella sp. SH-1 together with its genomic results offers new opportunities to examine biology, physiology, and biomineralization mechanisms of MTB.
Key words:    magnetotactic bacteria|magnetotaxis|pure culture|comparative genomic analysis   
Received: 2021-02-10   Revised: 2021-03-11
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References:
Altschul S F, Gish W, Miller W, Myers E W, Lipman D J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215(3):403-410, https://doi.org/10.1016/S0022-2836(05)80360-2.
Apweiler R, Bairoch A, Wu C H, Barker W C, Boeckmann B, Ferro S, Gasteiger E, Huang H Z, Lopez R, Magrane M, Martin M J, Natale D A, O'Donovan C, Redaschi N, Yeh L S L. 2004. UniProt:the Universal Protein knowledgebase. Nucleic Acids Research, 32(S1):D115-D119, https://doi.org/10.1093/nar/gkh131.
Arndt D, Grant J R, Marcu A, Sajed T, Pon A, Liang Y J, Wishart D S. 2016. PHASTER:a better, faster version of the PHAST phage search tool. Nucleic Acids Research, 44(W1):W16-W21, https://doi.org/10.1093/nar/gkw387.
Ashburner M, Ball C A, Blake J A, Botstein D, Butler H, Cherry J M, Davis A P, Dolinski K, Dwight S S, Eppig J T, Harris M A, Hill D P, Tarver L I, Kasarskis A, Lewis S, Matese J C, Richardson J E, Ringwald M, Rubin G M, Sherlock G. 2000. Gene Ontology:tool for the unification of biology. Nature Genetics, 25(1):25-29, https://doi.org/10.1038/75556.
Bazylinski D A, Blakemore R P. 1983. Denitrification and assimilatory nitrate reduction in Aquaspirillum magnetotacticum. Applied and Environmental Microbiology, 46(5):1118-1124, https://doi.org/10.1128/AEM.46.5.1118-1124.1983.
Bazylinski D A, Frankel R B, Heywood B R, Mann S, King J W, Donaghay P L, Hanson A K. 1995. Controlled biomineralization of magnetite (Fe3O4) and greigite(Fe3S4) in a magnetotactic bacterium. Applied and Environmental Microbiology, 61:3232-3239, https://doi.org/10.1128/AEM.61.9.3232-3239.1995.
Bazylinski D A, Frankel R B. 2004. Magnetosome formation in prokaryotes. Nature Reviews Microbiology, 2(3):217-230, https://doi.org/10.1038/nrmicro842.
Bazylinski D A, Williams T J, Lefèvre C T, Trubitsyn D, Fang J S, Beveridge T J, Moskowitz B M, Ward B, Schübbe S, Dubbels B L, Simpson B. 2013. Magnetovibrio blakemorei gen. nov., sp. nov., a magnetotactic bacterium(Alphaproteobacteria:Rhodospirillaceae) isolated from a salt marsh. International Journal of Systematic and Evolutionary Microbiology, 63(Pt 5):1824-1833, https://doi.org/10.1099/ijs.0.044453-0.
Benson G. 1999. Tandem repeats finder:a program to analyze DNA sequences. Nucleic Acids Research, 27(2):573-580, https://doi.org/10.1093/nar/27.2.573.
Blakemore R P, Maratea D, Wolfe R S. 1979. Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. Journal of Bacteriology, 140(2):720-729, https://doi.org/10.1128/JB.140.2.720-729.1979.
Blakemore R P. 1982. Magnetotactic bacteria. Annual Review of Microbiology, 36:217-238, https://doi.org/10.1146/annurev.mi.36.100182.001245.
Canchaya C, Proux C, Fournous G, Bruttin A, Brüssow H. 2003. Prophage genomics. Microbiology and Molecular Biology Reviews, 67(2):238-276, https://doi.org/10.1128/mmbr.67.2.238-276.2003.
Casjens S. 2003. Prophages and bacterial genomics:what have we learned so far? Molecular Microbiology, 49(2):277-300, https://doi.org/10.1046/j.1365-2958.2003.03580.x.
Consortium U P. 2015. UniProt:a hub for protein information. Nucleic Acids Research, 43(D1):D204-D212, https://doi.org/10.1093/nar/gku989.
DeLong E F, Frankel R B, Bazylinski D A. 1993. Multiple evolutionary origins of magnetotaxis in bacteria. Science, 259(5096):803-806, https://doi.org/10.1126/science.259.5096.803.
Du H J, Zhang W Y, Zhang W S, Zhang W J, Pan H M, Pan Y X, Bazylinski D A, Wu L F, Xiao T, Lin W. 2019. Magnetosome gene duplication as an important driver in the evolution of magnetotaxis in the Alphaproteobacteria. mSystems, 4(5):e00315-19, https://doi.org/10.1128/mSystems.00315-19.
Fouts D E. 2006. Phage_Finder:automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Research, 34(20):5839-5851, https://doi.org/10.1093/nar/gkl732.
Galperin M Y, Makarova K S, Wolf Y I, Koonin E V. 2015. Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Research, 43(D1):D261-D269, https://doi.org/10.1093/nar/gku1223.
Geurink C, Lefèvre C T, Monteil C L, Morillo-Lopez V, Abreu F, Bazylinski D A, Trubitsyn D. 2020. Complete genome sequence of strain BW-2, a magnetotactic gammaproteobacterium in the family Ectothiorhodospiraceae, isolated from a brackish spring in Death Valley, California. Microbiology Resource Announcements, 9(1):e01144-19, https://doi.org/10.1128/MRA.01144-19.
Grissa I, Vergnaud G, Pourcel C. 2007. CRISPRFinder:a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Research, 35(S2):W52-W57, https://doi.org/10.1093/nar/gkm360.
Grünberg K, Wawer C, Tebo B M, Schüler D. 2001. A large gene cluster encoding several magnetosome proteins is conserved in different species of magnetotactic bacteria. Applied and Environmental Microbiology, 67(10):4573-4582, https://doi.org/10.1128/aem.67.10.4573-4582.2001.
Hanzlik M, Winklhofer M, Petersen N. 2002. Pulsed-fieldremanence measurements on individual magnetotactic bacteria. Journal of Magnetism and Magnetic Materials, 248(2):258-267, https://doi.org/10.1016/S0304-8853(02)00353-0.
Hensen D, Sperling D, Trüper H G, Brune D C, Dahl C. 2006. Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Molecular Microbiology, 62(3):794-810, https://doi.org/10.1111/j.1365-2958.2006.05408.x.
Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter M C, Rattei T, Mende D R, Sunagawa S, Kuhn M, Jensen L J, von Mering C, Bork P. 2016. eggNOG 4.5:a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Research, 44(D1):D286-D293, https://doi.org/10.1093/nar/gkv1248.
Janssen D B, Pries F, van der Ploeg J, Kazemier B, Terpstra P, Witholt B. 1989. Cloning of 1,2-dichloroethane degradation genes of Xanthobacter autotrophicus GJ10 and expression and sequencing of the dhlA gene. Journal of Bacteriology, 171(12):6791-6799, https://doi.org/10.1128/jb.171.12.6791-6799.1989.
Ji B Y, Zhang S D, Arnoux P, Rouy Z, Alberto F, Philippe N, Murat D, Zhang W J, Rioux J B, Ginet N, Sabaty M, Mangenot S, Pradel N, Tian J S, Yang J, Zhang L C, Zhang W Y, Pan H M, Henrissat B, Coutinho P M, Li Y, Xiao T, Médigue C, Barbe V, Pignol D, Talla E, Wu L F. 2014. Comparative genomic analysis provides insights into the evolution and niche adaptation of marine Magnetospira sp. QH-2 strain. Environmental Microbiology, 16(2):525-544, https://doi.org/10.1111/1462-2920.12180.
Ji B Y, Zhang S D, Zhang W J, Rouy Z, Alberto F, Santini C L, Mangenot S, Gagnot S, Philippe N, Pradel N, Zhang L C, Tempel S, Li Y, Médigue C, Henrissat B, Coutinho P M, Barbe V, Talla E, Wu L F. 2017. The chimeric nature of the genomes of marine magnetotactic coccoid-ovoid bacteria defines a novel group of Proteobacteria. Environmental Microbiology, 19(3):1103-1119, https://doi.org/10.1111/1462-2920.13637.
Jogler C, Schüler D. 2009. Genomics, genetics, and cell biology of magnetosome formation. Annual Review of Microbiology, 63:501-521, https://doi.org/10.1146/annurev.micro.62.081307.162908.
Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. 2016. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Research, 44(D1):D457-D462, https://doi.org/10.1093/nar/gkv1070.
Kolinko S, Jogler C, Katzmann E, Wanner G, Peplies J, Schüler D. 2012. Single-cell analysis reveals a novel uncultivated magnetotactic bacterium within the candidate division OP3. Environmental Microbiology, 14(7):1709-1721, https://doi.org/10.1111/j.1462-2920.2011.02609.x.
Kuypers M M M, Marchant H K, Kartal B. 2018. The microbial nitrogen-cycling network. Nature Reviews Microbiology, 16(5):263-276, https://doi.org/10.1038/nrmicro.2018.9.
Lefèvre C T, Abreu F, Schmidt M L, Lins U, Frankel R B, Hedlund B P, Bazylinski D A. 2010. Moderately thermophilic magnetotactic bacteria from hot springs in Nevada. Applied and Environmental Microbiology, 76(11):3740-3743, https://doi.org/10.1128/AEM.03018-09.
Lefèvre C T, Bazylinski D A. 2013. Ecology, diversity, and evolution of magnetotactic bacteria. Microbiology and Molecular Biology Reviews, 77(3):497-526, https://doi.org/10.1128/MMBR.00021-13.
Lefèvre C T, Bernadac A, Yu-Zhang K, Pradel N, Wu L F. 2009. Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. Environmental Microbiology, 11(7):1646-1657, https://doi.org/10.1111/j.1462-2920.2009.01887.x.
Li Y J, Katzmann E, Borg S, Schüler D. 2012. The periplasmic nitrate reductase nap is required for anaerobic growth and involved in redox control of magnetite biomineralization in Magnetospirillum gryphiswaldense. Journal of Bacteriology, 194(18):4847-4856, https://doi.org/10.1128/JB.00903-12.
Lin W, Pan Y X, Bazylinski D A. 2017a. Diversity and ecology of and biomineralization by magnetotactic bacteria. Environmental Microbiology Reports, 9(4):345-356, https://doi.org/10.1111/1758-2229.12550.
Lin W, Pan Y X. 2015. A putative greigite-type magnetosome gene cluster from the candidate phylum Latescibacteria. Environmental Microbiology Reports, 7(2):237-242, https://doi.org/10.1111/1758-2229.12234.
Lin W, Paterson G A, Zhu Q Y, Wang Y Z, Kopylova E, Li Y, Knight R, Bazylinski D A, Zhu R X, Kirschvink J L, Pan Y X. 2017b. Origin of microbial biomineralization and magnetotaxis during the Archean. Proceedings of the National Academy of Sciences of the United States of America, 114(9):2171-2176, https://doi.org/10.1073/pnas.1614654114.
Lin W, Zhang W S, Paterson G A, Zhu Q Y, Zhao X, Knight R, Bazylinski D A, Roberts A P, Pan Y X. 2020. Expanding magnetic organelle biogenesis in the domain Bacteria. Microbiome, 8(1):152, https://doi.org/10.1186/s40168-020-00931-9.
Lin W, Zhang W S, Zhao X, Roberts A P, Paterson G A, Bazylinski D A, Pan Y X. 2018. Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with lineage-specific evolution. The ISME Journal, 12(6):1508-1519, https://doi.org/10.1038/s41396-018-0098-9.
Lohße A, Ullrich S, Katzmann E, Borg S, Wanner G, Richter M, Voigt B, Schweder T, Schüler D. 2011. Functional analysis of the magnetosome island in Magnetospirillum gryphiswaldense:the mamAB operon is sufficient for magnetite biomineralization. PLoS One, 6(10):e25561, https://doi.org/10.1371/journal.pone.0025561.
Makarova K S, Wolf Y I, Koonin E V. 2015. Archaeal clusters of orthologous genes (arcogs):an update and application for analysis of shared features between thermococcales, methanococcales, and methanobacteriales. Life, 5(1):818-840, https://doi.org/10.3390/life5010818.
Maratea D, Blakemore R P. 1981. Aquaspirillum magnetotacticum sp. nov., a magnetic spirillum. International Journal of Systematic and Evolutionary Microbiology, 31(4):452-455, https://doi.org/10.1099/00207713-31-4-452.
Matsunaga T, Okamura Y, Fukuda Y, Wahyudi A T, Murase Y, Takeyama H. 2005. Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA Research, 12(3):157-166, https://doi.org/10.1093/dnares/dsi002.
Matsunaga T, Sakaguchi T, Tadakoro F. 1991. Magnetite formation by a magnetic bacterium capable of growing aerobically. Applied Microbiology and Biotechnology, 35(5):651-655, https://doi.org/10.1007/BF00169632.
Matsunaga T, Tsujimura N. 1993. Respiratory inhibitors of a magnetic bacterium Magnetospirillum sp. AMB-1 capable of growing aerobically. Applied Microbiology and Biotechnology, 39(3):368-371, https://doi.org/10.1007/BF00192094.
Miele V, Penel S, Duret L. 2011. Ultra-fast sequence clustering from similarity networks with SiLiX. BMC Bioinformatics, 12:116, https://doi.org/10.1186/1471-2105-12-116.
Monteil C L, Perrière G, Menguy N, Ginet N, Alonso B, Waisbord B, Cruveiller S, Pignol D, Lefèvre C T. 2018. Genomic study of a novel magnetotactic Alphaproteobacteria uncovers the multiple ancestry of magnetotaxis. Environmental Microbiology, 20(12):4415-4430, https://doi.org/10.1111/1462-2920.14364.
Murat D, Quinlan A, Vali H, Komeili A. 2010. Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proceedings of the National Academy of Sciences of the United States of America, 107(12):5593-5598, https://doi.org/10.1073/pnas.0914439107.
Paul J H. 2008. Prophages in marine bacteria:dangerous molecular time bombs or the key to survival in the seas? The ISME Journal, 2(6):579-589, https://doi.org/10.1038/ismej.2008.35.
Pinto R, Tang Q X, Britton W J, Leyh T S, Triccas J A. 2004. The Mycobacterium tuberculosis cysD and cysNC genes form a stress-induced operon that encodes a tri-functional sulfate-activating complex. Microbiology, 150(6):1681-1686, https://doi.org/10.1099/mic.0.26894-0.
Richter M, Kube M, Bazylinski D A, Lombardot T, Glöckner F O, Reinhardt R, Schüler D. 2007. Comparative genome analysis of four magnetotactic bacteria reveals a complex set of group-specific genes implicated in magnetosome biomineralization and function. Journal of Bacteriology, 189(13):4899-4910, https://doi.org/10.1128/JB.00119-07.
Rioux J B, Philippe N, Pereira S, Pignol D, Wu L F, Ginet N. 2010. A second actin-like MamK protein in Magnetospirillum magneticum AMB-1 encoded outside the genomic magnetosome island. PLoS One, 5(2):e9151, https://doi.org/10.1371/journal.pone.0009151.
Sakaguchi T, Arakaki A, Matsunaga T. 2002. Desulfovibrio magneticus sp. nov., a novel sulfate-reducing bacterium that produces intracellular single-domain-sized magnetite particles. International Journal of Systematic and Evolutionary Microbiology, 52(Pt 1):215-221, https://doi.org/10.1099/00207713-52-1-215.
Schleifer K H, Schüler D, Spring S, Weizenegger M, Amann R, Ludwig W, Köhler M. 1991. The genus Magnetospirillum gen. nov. description of Magnetospirillum gryphiswaldense sp. nov. and transfer of Aquaspirillum magnetotacticum to Magnetospirillum magnetotacticum comb. nov. 1. Systematic and Applied Microbiology, 14(4):379-385, https://doi.org/10.1016/s0723-2020(11)80313-9.
Schübbe S, Williams T J, Xie G, Kiss H E, Brettin T S, Martinez D, Ross C A, Schüler D, Cox B L, Nealson K H, Bazylinski D A. 2009. Complete genome sequence of the chemolithoautotrophic marine magnetotactic coccus strain MC-1. Applied Environmental Microbiology, 75(14):4835-4852, https://doi.org/10.1128/AEM.02874-08.
Simmons S L, Sievert S M, Frankel R B, Bazylinski D A, Edwards K J. 2004. Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Applied and Environmental Microbiology, 70(10):6230-6239, https://doi.org/10.1128/AEM.70.10.6230-6239.2004.
Touchon M, Bernheim A, Rocha E P C. 2016. Genetic and lifehistory traits associated with the distribution of prophages in bacteria. The ISME Journal, 10(11):2744-2754, https://doi.org/10.1038/ismej.2016.47.
Touchon M, de Sousa J A M, Rocha E P C. 2017. Embracing the enemy:the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer. Current Opinion in Microbiology, 38:66-73, https://doi.org/10.1016/j.mib.2017.04.010.
Trubitsyn D, Monteil C L, Geurink C, Morillo-Lopez V, de Almeida L G P, de Vasconcelos T R, Abreu F, Bazylinski D A, Lefevre C T. 2021. Complete genome sequence of strain SS-5, a magnetotactic gammaproteobacterium isolated from the Salton Sea, a Shallow, Saline, Endorheic Rift Lake located on the San Andreas Fault in California. Microbiology Resource Announcements, 10(1):e00928-20, https://doi.org/10.1128/MRA.00928-20.
Uebe R, Schüler D, Jogler C, Wiegand S. 2018. Reevaluation of the complete genome sequence of Magnetospirillum gryphiswaldense MSR-1 with single-molecule real-time sequencing data. Genome Announcements, 6(17):e00309-18, https://doi.org/10.1128/genomeA.00309-18.
Uzun M, Alekseeva L, Krutkina M, Koziaeva V, Grouzdev D. 2020. Unravelling the diversity of magnetotactic bacteria through analysis of open genomic databases. Scientific Data, 7(1):252, https://doi.org/10.1038/s41597-020-00593-0.
Vali H, Förster O, Amarantidis G, Petersen N. 1987. Magnetotactic bacteria and their magnetofossils in sediments. Earth and Planetary Science Letters, 86(2-4):389-400, https://doi.org/10.1016/0012-821X(87)90235-4.
Vallenet D, Belda E, Calteau A, Cruveiller S, Engelen S, Lajus A, Le Fèvre F, Longin C, Mornico D, Roche D, Rouy Z, Salvignol G, Scarpelli S, Smith A A T, Weiman M, Médigue C. 2013. MicroScope-an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Research, 41(D1):D636-D647, https://doi.org/10.1093/nar/gks1194.
Verschueren K H G, Franken S M, Rozeboom H J, Kalk K H, Dijkstra B W. 1993. Refined X-ray structures of haloalkane dehalogenase at pH 6.2 and pH 8.2 and implications for the reaction mechanism. Journal of Molecular Biology, 232(3):856-872, https://doi.org/10.1006/jmbi.1993.1436.
Wang Y Z, Zhang T W, Lin W, Zhang B F, Cai Y, Yang C Y, Li J H, Xu H T, Pan Y X. 2016. Complete genome sequence of Magnetospirillum sp. strain XM-1, isolated from the Xi'an City moat, China. Genome Announcements, 4(5):e01171-16, https://doi.org/10.1128/genomeA.01171-16.
Wenter R, Wanner G, Schüler D, Overmann J. 2009. Ultrastructure, tactic behaviour and potential for sulfate reduction of a novel multicellular magnetotactic prokaryote from North Sea sediments. Environmental Microbiology, 11(6):1493-1505, https://doi.org/10.1111/j.1462-2920.2009.01877.x.
Williams T J, Lefèvre C T, Zhao W D, Beveridge T J, Bazylinski D A. 2012. Magnetospira thiophila gen. nov., sp. nov., a marine magnetotactic bacterium that represents a novel lineage within the Rhodospirillaceae(Alphaproteobacteria). International Journal of Systematic and Evolutionary Microbiology, 62(Pt 10):2443-2450, https://doi.org/10.1099/ijs.0.037697-0.
Yang C D, Takeyama H, Tanaka T, Matsunaga T. 2001. Effects of growth medium composition, iron sources and atmospheric oxygen concentrations on production of luciferase-bacterial magnetic particle complex by a recombinant Magnetospirillum magneticum AMB-1. Enzyme and Microbial Technology, 29(1):13-19, https://doi.org/10.1016/S0141-0229(01)00343-X.
Zhou K, Zhang W Y, Pan H M, Li J H, Yue H D, Xiao T, Wu L F. 2013. Adaptation of spherical multicellular magnetotactic prokaryotes to the geochemically variable habitat of an intertidal zone. Environmental Microbiology, 15(5):1595-1605, https://doi.org/10.1111/1462-2920.12057.
Zhu K L, Pan H M, Li J H, Yu-Zhang K, Zhang S D, Zhang W Y, Zhou K, Yue H D, Pan Y X, Xiao T, Wu L F. 2010. Isolation and characterization of a marine magnetotactic spirillum axenic culture QH-2 from an intertidal zone of the China Sea. Research in Microbiology, 161(4):276-283, https://doi.org/10.1016/j.resmic.2010.02.003.
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