Distribution and diversity of magnetotactic bacteria in sediments of the Yellow Sea continental shelf

Sediments, Sec 4 • Sediment-Ecology Interactions • Research Article
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Abstract

Purpose

Magnetotactic bacteria (MTB) are cosmopolitan and ubiquitous in sediments of freshwater and marine habitats. Most studies of marine MTB have concerned intertidal zones, and there have been few reports of MTB from seafloor sediments. The objective of this study was to investigate the diversity and spatial distribution of MTB on the continent shelf of the Yellow Sea.

Materials and methods

Sediments from the continental shelf were collected from the Yellow Sea in August 2015 (summer) and January 2016 (winter). Magnetotactic bacteria were enriched by a permanent magnet. The number of MTB was counted. The diversity of MTB was identified based on high-throughput sequencing and Silva database and nt/nr database. Environmental factors including bottom temperature and salinity, total carbon (TC), total nitrogen (TN), total sulfur (TS), total organic carbon (TOC), concentration of iron, and the sediment grain size were measured.

Results and discussion

Magnetotactic bacteria were distributed widely in the Yellow Sea, at abundances of 5–2400 ind./dm3 in summer and 5–820 ind./dm3 in winter. The dominant MTB at most sampling stations were cocci, although rod-shaped MTB dominated at one station (H17). High-throughput sequencing distinguished 2669 reads for putative MTB in summer and 3271 in winter, and these were classified into 72 operational taxonomic units (OTUs). In both summer and winter, most reads (> 74%) and OTUs (> 50%) of putative MTB belonged to the Nitrospirae. The MTB abundance was significantly correlated with sediment grain size. The MTB abundance was highest at station H17, where the sediment grain size was larger than at other stations.

Conclusions

We present a systematic assessment of the spatial distribution and diversity of MTB in sediments of the continental shelf of the Yellow Sea. Our data suggest that diverse MTB are widely distributed in the seafloor sediment of the Yellow Sea, with Nitrospirae likely being the dominating group, and that the abundance of MTB are influenced by sediment grain size.

Keywords

Continental shelf Magnetotactic bacteria Nitrospirae Spatial distribution Sediment grain size Yellow Sea 

Notes

Acknowledgements

We thank Yi Dong, Jia Liu, and Zhao-Jie Teng for their helpful discussions, and Ming Jiang and Xi-Cheng Ma for aiding with our TEM observations and EDXS analysis. This work was supported by the National Natural Science Foundation of China (41776131, 41330962 and 41776130) and the National Natural Science Foundation of China—Shandong Joint Fund (U1606404 and U1706208).

Supplementary material

11368_2018_1912_MOESM1_ESM.docx (1.8 mb)
ESM 1 (DOCX 1867 kb).

References

  1. Abreu F, Martins JL, Silveira TS, Keim CN, Lins de Barros HGP, Filho FJG, Lins U (2007) Candidatus Magnetoglobus multicellularis’, a multicellular, magnetotactic prokaryote from a hypersallne environment. Int J Syst Evol Microbiol 57(6):1318–1322.  https://doi.org/10.1099/ijs.0.64857-0
  2. Alve E (1999) Colonization of new habitats by benthic foraminifera: a review. Earth-Sci Rev 46(1-4):167–185.  https://doi.org/10.1016/S0012-8252(99)00016-1CrossRefGoogle Scholar
  3. Amann R, Peplies J, Schüler D (2007) Diversity and taxonomy of magnetotactic bacteria. In: Schüler D (ed) Magnetoreception and magnetosomes in bacteria. Springer, Berlin, Heidelberg, pp 25–36.  https://doi.org/10.1007/7171_037CrossRefGoogle Scholar
  4. Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19(24):5555–5565.  https://doi.org/10.1111/j.1365-294X.2010.04898.xCrossRefGoogle Scholar
  5. Armynot du Chatelet E, Bout-Roumazeilles V, Riboulleau A, Trentesaux A (2009) Sediment (grain size and clay mineralogy) and organic matter quality control on living benthic foraminifera. Rev Micropaleontol 52(1):75–84.  https://doi.org/10.1016/j.revmic.2008.10.002CrossRefGoogle Scholar
  6. Bahaj AS, James PAB, Croudace IW (1994) Metal uptake and separation using magnetotactic bacteria. IEEE Trans Magn 30(6):4707–4709.  https://doi.org/10.1109/20.334196CrossRefGoogle Scholar
  7. Bazylinski DA, Frankel RB, Jannasch HW (1988) Anaerobic magnetite production by a marine, magnetotactic bacterium. Nature 334(6182):518–519.  https://doi.org/10.1038/334518a0CrossRefGoogle Scholar
  8. Bazylinski DA (1996) Controlled biomineralization of magnetic minerals by magnetotactic bacteria. Chem Geol 132(1-4):191–198.  https://doi.org/10.1016/S0009-2541(96)00055-1CrossRefGoogle Scholar
  9. Bazylinski DA (1999) Synthesis of the bacterial magnetosome: the making of a magnetic personality. Int Microbiol 2(2):71–80Google Scholar
  10. Bazylinski DA, Frankel RB (2004) Magnetosome formation in prokaryotes. Nat Rev Microbiol 2(3):217–230.  https://doi.org/10.1038/nrmicro842CrossRefGoogle Scholar
  11. Bazylinski DA, Lefèvre CT, Schüler D (2013) Magnetotactic bacteria. In: Rosenberg E, Delong E, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer-Verlag, Berlin Heidelberg, pp 453–494.  https://doi.org/10.1007/978-3-642-30141-4_74CrossRefGoogle Scholar
  12. Cangemi M, Bellanca A, Borin S, Hopkinson L, Mapelli F, Neri R (2010) The genesis of actively growing siliceous stromatolites: evidence from Lake Specchio di Venere, Pantelleria Island, Italy. Chem Geol 276(3-4):318–330.  https://doi.org/10.1016/j.chemgeo.2010.06.017CrossRefGoogle Scholar
  13. Chen Y, Zhang R, Du H, Pan H, Zhang W, Zhou K, Li J, Xiao T, Wu L-F (2015) A novel species of ellipsoidal multicellular magnetotactic prokaryotes from Lake Yuehu in China. Environ Microbiol 17(3):637–647.  https://doi.org/10.1111/1462-2920.12480
  14. Chen Y, Zhang W, Zhou K, Pan H, Du H, Xu C, Xu J, Pradel N, Santini CL, Li J, Huang H, Pan Y, Xiao T, Wu L-F (2016) Novel species and expanded distribution of ellipsoidal multicellular magnetotactic prokaryotes. Environ Microbiol Rep 8(2):218–226.  https://doi.org/10.1111/1758-2229.12371
  15. Dai X, Zhou H, Chen Y, Cai C, Zhou Y, Zhou S, Qu L (2002) Diversity of bacteria in sediments of Nansha sea area of South China Sea. Prog Nat Sci 12:479–484 (in Chinese)Google Scholar
  16. Debenay JP, Tsakiridis E, Soulard R, Grossel H (2001) Factors determining the distribution of foraminiferal assemblages in Port Joinville Harbor (Ile d’Yeu, France): the influence of pollution. Mar Micropaleontol 43(1-2):75–118.  https://doi.org/10.1016/S0377-8398(01)00023-8CrossRefGoogle Scholar
  17. Diz P, Frances G, Costas S, Souto C, Alejo I (2004) Distribution of benthic foraminifera in coarse sediments, Ría de Vigo, NW Iberian margin. J Foramin Res 34(4):258–275.  https://doi.org/10.2113/34.4.258CrossRefGoogle Scholar
  18. Dong Y, Li J, Zhang WC, Zhang W, Zhao Y, Xiao T, Wu L-F, Pan H (2016) The detection of magnetotactic bacteria in deep sea sediments from the east Pacific Manganese Nodule Province. Environ Microbiol Rep 8(2):239–249.  https://doi.org/10.1111/1758-2229.12374
  19. Du H, Chen Y, Zhang R, Pan H, Zhang W, Zhou K, Wu L-F, Xiao T (2015) Temporal distributions and environmental adaptations of two types of multicellular magnetotactic prokaryote in the sediments of Lake Yuehu, China. Environ Microbiol Rep 7(3):538–546.  https://doi.org/10.1111/1758-2229.12284
  20. Flies CB, Jonkers HM, de Beer D, Bosselmann K, Bottcher ME, Schüler D (2005a) Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiol Ecol 52(2):185–195.  https://doi.org/10.1016/j.femsec.2004.11.006CrossRefGoogle Scholar
  21. Flies CB, Peplies J, Schüler D (2005b) Combined approach for characterization of uncultivated magnetotactic bacteria from various aquatic environments. Appl Environ Microbiol 71(5):2723–2731.  https://doi.org/10.1128/AEM.71.5.2723-2731.2005CrossRefGoogle Scholar
  22. Fuduche M, Postec A, Davidson S, Chauvin JP, Galès G, Hirschler-Réa A, Ollivier B, Wu L-F, Pradel N (2015) Diversity of magnetotactic bacteria from a French pristine Mediterranean area. Curr Microbiol 70(4):499–505.  https://doi.org/10.1007/s00284-014-0745-y
  23. 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. Environ Microbiol 14(7):1709–1721.  https://doi.org/10.1111/j.1462-2920.2011.02609.xCrossRefGoogle Scholar
  24. Lagkouvardos I, Jehl MA, Rattei T, Horn M (2014) Signature protein of the PVC superphylum. Appl Environ Microbiol 80(2):440–445.  https://doi.org/10.1128/AEM.02655-13CrossRefGoogle Scholar
  25. Lefèvre CT, Bazylinski DA (2013) Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol Mol Biol Rev 77(3):497–526.  https://doi.org/10.1128/MMBR.00021-13CrossRefGoogle Scholar
  26. Lefèvre CT, Frankel RB, Abreu F, Lins U, Bazylinski DA (2011) Culture-independent characterization of a novel, uncultivated magnetotactic member of the Nitrospirae phylum. Environ Microbiol 13(2):538–549.  https://doi.org/10.1111/j.1462-2920.2010.02361.xCrossRefGoogle Scholar
  27. Lefèvre CT, Viloria N, Schmidt ML, Pósfai M, Frankel RB, Bazylinski DA (2012) Novel magnetite-producing magnetotactic bacteria belonging to the Gammaproteobacteria. ISME J 6(2):440–450.  https://doi.org/10.1038/ismej.2011.97CrossRefGoogle Scholar
  28. Lin W, Li J, Schüler D, Jogler C, Pan Y (2009) Diversity analysis of magnetotactic bacteria in Lake Miyun, northern China, by restriction fragment length polymorphism. Syst Appl Microbiol 32(5):342–350.  https://doi.org/10.1016/j.syapm.2008.10.005CrossRefGoogle Scholar
  29. Lin W, Pan Y (2010) Temporal variation of magnetotactic bacterial communities in two freshwater sediment microcosms. FEMS Microbiol Lett 302(1):85–92.  https://doi.org/10.1111/j.1574-6968.2009.01838.xCrossRefGoogle Scholar
  30. Lin W, Pan Y (2015) A putative greigite-type magnetosome gene cluster from the candidate phylum Latescibacteria. Environ Microbiol Rep 7(2):237–242.  https://doi.org/10.1111/1758-2229.12234CrossRefGoogle Scholar
  31. Lin W, Wang Y, Gorby Y, Nealson K, Pan Y (2013) Integrating niche-based process and spatial process in biogeography of magnetotactic bacteria. Sci Rep 3(1):1643.  https://doi.org/10.1038/srep01643CrossRefGoogle Scholar
  32. Lin W, Wang Y, Li B, Pan Y (2012a) A biogeographic distribution of magnetotactic bacteria influenced by salinity. ISME J 6(2):475–479.  https://doi.org/10.1038/ismej.2011.112CrossRefGoogle Scholar
  33. Lin W, Wang Y, Pan Y (2012b) Short-term effects of temperature on the abundance and diversity of magnetotactic cocci. Microbiology 1:53–63Google Scholar
  34. Liu J, Liu X, Wang M, Qiao Y, Zheng Y, Zhang X (2015) Bacterial and archaeal communities in sediments of the north Chinese marginal seas. Microb Ecol 70(1):105–117.  https://doi.org/10.1007/s00248-014-0553-8CrossRefGoogle Scholar
  35. Mann S, Sparks NHC (1990) Magnetotactic bacteria-microbiology, biomineralization, paleomagnetism and biotechnology. Adv Microb Physiol 31:125–181.  https://doi.org/10.1016/S0065-2911(08)60121-6CrossRefGoogle Scholar
  36. Martins JL, Silveira TS, Abreu F, de Almeida FP, Rosado AS, Lins U (2012) Spatiotemporal distribution of the magnetotactic multicellular prokaryote Candidatus Magnetoglobus multicellularis in a Brazilian hypersaline lagoon and in microcosms. Int Microbiol 15(3):141–149.  https://doi.org/10.2436/20.1501.01.167Google Scholar
  37. Martins JL, Silveira TS, Silva KT, Lins U (2009) Salinity dependence of the distribution of multicellular magnetotactic prokaryotes in a hypersaline lagoon. Int Microbiol 12(3):193–201Google Scholar
  38. Pan H, Zhu K, Song T, Yu-Zhang K, Lefèvre C, Xing S, Liu M, Zhao S, Xiao T, Wu L-F (2008) Characterization of a homogeneous taxonomic group of marine magnetotactic cocci within a low tide zone in the China Sea. Environ Microbiol 10(5):1158–1164.  https://doi.org/10.1111/j.1462-2920.2007.01532.x
  39. Petermann H, Bleil U (1993) Detection of live magnetotactic bacteria in South Atlantic deep-sea sediments. Earth Planet Sci Lett 117(1-2):223–228.  https://doi.org/10.1016/0012-821X(93)90128-VCrossRefGoogle Scholar
  40. Petersen N, Weiss DG, Vali H (1989) Magnetic bacteria in lake sediments. In: Lowes FJ, Collinson DW, Parry JH, Runcorn SK, Tozer DC, Soward A (eds) Geomagnetism and palaeomagnetism. Springer, Dordrecht, pp 231–241.  https://doi.org/10.1007/978-94-009-0905-2_17CrossRefGoogle Scholar
  41. Postec A, Tapia N, Bernadac A, Joseph M, Davidson S, Wu L-F, Ollivier B, Pradel N (2012) Magnetotactic bacteria in microcosms originating from the French Mediterranean coast subjected to oil industry activities. Microb Ecol 63(1):1–11.  https://doi.org/10.1007/s00248-011-9910-z
  42. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(Database issue):D590–D596.  https://doi.org/10.1093/nar/gks1219Google Scholar
  43. Rotaru C, Woodard TL, Choi S, Nevin KP (2012) Spatial heterogeneity of bacterial communities in sediments from an infiltration basin receiving highway runoff. Microb Ecol 64(2):461–473.  https://doi.org/10.1007/s00248-012-0026-xCrossRefGoogle Scholar
  44. Simmons SL, Sievert SM, Frankel RB, Bazylinski DA, Edwards KJ (2004) Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Appl Environ Microbiol 70(10):6230–6239.  https://doi.org/10.1128/AEM.70.10.6230-6239.2004CrossRefGoogle Scholar
  45. Sobrinho RL, Lins U, Bernardes MC (2011) Geochemical characteristics related to the gregite-producing multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis in a hypersaline lagoon. Geomicrobiol J 28(8):705–713.  https://doi.org/10.1080/01490451.2010.514027CrossRefGoogle Scholar
  46. Spring S, Amann R, Ludwig W, Schleifer KH, Schüler D, Poralla K, Petersen N (1995) Phylogenetic analysis of uncultured magnetotactic bacteria from the alpha-subclass of Proteobacteria. Syst Appl Microbiol 17(4):501–508.  https://doi.org/10.1016/S0723-2020(11)80068-8CrossRefGoogle Scholar
  47. Stolz JF, Chang SBR, Kirschvink JL (1986) Magnetotactic bacteria and single-domain magnetite in hemipelagic sediments. Nature 321(6073):849–851.  https://doi.org/10.1038/321849a0CrossRefGoogle Scholar
  48. Vali H, Tv D, Amarantidis G, Förster O, Morteani G, Bachmann L, Petersen N (1989) Biogenic and lithogenic magnetic minerals in Atlantic and Pacific deep sea sediments and their paleomagnetic significance. Geol Rundsch 78(3):753–764.  https://doi.org/10.1007/BF01829320CrossRefGoogle Scholar
  49. Vali H, Förster O, Amarantidis G, Petersen N (1987) Magnetotactic bacteria and their magnetofossils in sediments. Earth Planet Sci Lett 86(2-4):389–400.  https://doi.org/10.1016/0012-821X(87)90235-4CrossRefGoogle Scholar
  50. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267.  https://doi.org/10.1128/AEM.00062-07CrossRefGoogle Scholar
  51. Williams TJ, Zhang CL, Scott JH, Bazylinski DA (2006) Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1. Appl Environ Microbiol 72(2):1322–1329.  https://doi.org/10.1128/AEM.72.2.1322-1329.2006CrossRefGoogle Scholar
  52. Zhang R, Chen Y, Zhou K, Zhang W, Xiao T, Wu L-F (2013a) Vertical distribution characteristics of magnetotactic bacteria and the relationship with environmental factors in intertidal zone of Qingdao. Mar Sci 37:24–31 (in Chinese with English abstract)Google Scholar
  53. Zhang W, Zhou K, Pan H, Du H, Chen Y, Zhang R, Ye W, Lu C, Xiao T, Wu L-F (2013b) Novel rod-shaped magnetotactic bacteria belonging to the class Alphaproteobacteria. Appl Environ Microbiol 79(9):3137–3140.  https://doi.org/10.1128/AEM.03869-12
  54. Zhao Y, Yu D (1983) Geochemical analysis of the sediments of the Huanghai Sea. Haiyang Yu Huzhao 14:433–446 (in Chinese)Google Scholar
  55. Zhu K, Pan H, Li J, Yu-Zhang K, Zhang S, Zhang W, Zhou K, Yue H, Pan Y, 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. Res Microbiol 161(4):276–283.  https://doi.org/10.1016/j.resmic.2010.02.003

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.CAS Key Laboratory of Marine Ecology and Environmental SciencesInstitute of Oceanology, Chinese Academy of SciencesQingdaoChina
  2. 2.Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.International Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms (LIA-MagMC), CNRS-CASQingdaoChina

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