Microbial Ecology

, Volume 78, Issue 4, pp 804–819 | Cite as

Heterotrophic Bacteria Dominate the Diazotrophic Community in the Eastern Indian Ocean (EIO) during Pre-Southwest Monsoon

  • Chao Wu
  • Jinjun Kan
  • Haijiao Liu
  • Laxman Pujari
  • Congcong Guo
  • Xingzhou Wang
  • Jun SunEmail author
Microbiology of Aquatic Systems


The diazotrophic communities play an important role in sustaining primary productivity through adding new nitrogen to oligotrophic marine ecosystems. Yet, their composition in the oligotrophic Indian Ocean is poorly understood. Here, we report the first observation of phylogenetic diversity and distribution of diazotrophs in the Eastern Indian Ocean (EIO) surface water (to 200 m) during the pre-southwest monsoon period. Through high throughput sequencing of nifH genes, we identified diverse groups of diazotrophs in the EIO including both non-cyanobacterial and cyanobacterial phylotypes. Proteobacteria (mainly Alpha-, Beta-, and Gamma-proteobacteria) were the most diverse and abundant groups within all the diazotrophs, which accounted for more than 86.9% of the total sequences. Cyanobacteria were also retrieved, and they were dominated by the filamentous non-heterocystous cyanobacteria Trichodesmium spp. Other cyanobacteria such as unicellular diazotrophic cyanobacteria were detected sporadically. Interestingly, our qPCR analysis demonstrated that the depth-integrated gene abundances of the diazotrophic communities exhibited spatial heterogeneity with Trichodesmium spp. appeared to be more abundant in the Bay of Bengal (p < 0.05), while Sagittula castanea (Alphaproteobacteria) was found to be more dominating in the equatorial region and offshores (p < 0.05). Non-metric multidimensional scaling analysis (NMDS) further confirmed distinct vertical and horizontal spatial variations in the EIO. Canonical correspondence analysis (CCA) indicated that temperature, salinity, and phosphate were the major environmental factors driving the distribution of the diazotroph communities. Overall, our study provides the first insight into the diversity and distribution of the diazotrophic communities in EIO. The findings from this study highlight distinct contributions of both non-cyanobacteria and cyanobacteria to N2 fixation. Moreover, our study reveals information that is critical for understanding spatial heterogeneity and distribution of diazotrophs, and their vital roles in nitrogen and carbon cycling.


Diazotroph Heterotrophic bacteria Trichodesmium High throughput sequencing Nitrogen fixation The eastern Indian Ocean 



We thank Prof. Dongxiao Wang from South China Sea Institute of Oceanology, Chinese Academy of Sciences for providing hydrographic (CTD) data. Dr. Liangliang Kong at McGill University and Dr. Xiaomin Xia at the Hong Kong University of Science and Technology are also acknowledged for their help and technical support during experiments. We also gratefully acknowledge the crew of R/V “Shiyan 3” and all participants for their assistance during the cruise.

Author Contributions

This work was designed by JS. Samples were collected by CW, HL, and XW. CW performed experiments and analyzed data. CG performed the nutrients analysis. CW drafted the paper and revised by JK and PL. All authors contributed to the writing of the manuscript.

Funding Information

This study was supported by the National Natural Science Foundation of China (41876134, 41276124, and 41676112) and NSFC open research cruises (NORC2017-10), the Science Fund for University Creative Research Groups in Tianjin (TD12-5003), the Changjiang Scholar Program of Chinese Ministry of Education to JS, and endowment support from Stroud Water Research Center to JK.

Supplementary material

248_2019_1355_Fig9_ESM.png (5.2 mb)
Fig. S1

Depth profiles of dissolved inorganic nutrients (nitrate, nitrite, ammonium, phosphate, silicate) and Chl a in the EIO (PNG 5281 kb)

248_2019_1355_MOESM1_ESM.tif (1.5 mb)
High resolution image (TIF 1530 kb)
248_2019_1355_Fig10_ESM.png (1.2 mb)
Fig. S2

Rarefaction curves comparing the number of reads with the number of phylotypes (OTUs) found in the DNA libraries in the EIO. The last digit represented water depth: 1, 2 and 3 represent 0m, 75m and 200m, respectively. (PNG 1240 kb)

248_2019_1355_MOESM2_ESM.tif (2.6 mb)
High resolution image (TIF 2708 kb)
248_2019_1355_MOESM3_ESM.docx (23 kb)
Supplementary Table 1 (DOCX 22 kb)


  1. 1.
    Dugdale RC, Goering JJ (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol Oceanogr 12:196–206. CrossRefGoogle Scholar
  2. 2.
    Zehr JP (2011) Nitrogen fixation by marine cyanobacteria. Trends Microbiol 19:162–173. CrossRefPubMedGoogle Scholar
  3. 3.
    Gradoville MR, Bombar D, Crump BC, Letelier RM, Zehr JP, White AE (2017) Diversity and activity of nitrogen-fixing communities across ocean basins. Limnol Oceanogr 62:1895–1909. CrossRefGoogle Scholar
  4. 4.
    Levitan O, Rosenberg G, Setlik I et al (2007) Elevated CO2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob Chang Biol 13:531–538. CrossRefGoogle Scholar
  5. 5.
    Benavides M, Voss M (2015) Five decades of N2 fixation research in the North Atlantic Ocean. Front Mar Sci 2:1–40. CrossRefGoogle Scholar
  6. 6.
    Yang L, Wang DX, Huang J, Wang X, Zeng L, Shi R, He Y, Xie Q, Wang S, Chen R, Yuan J, Wang Q, Chen J, Zu T, Li J, Sui D, Peng S (2015) Toward a mesoscale hydrological and marine meteorological observation network in the South China Sea. Bull Am Meteorol Soc 96(7):1117–1135. CrossRefGoogle Scholar
  7. 7.
    Carpenter EJ, Subramaniam A, Capone DG (2004) Biomass and primary productivity of the cyanobacterium Trichodesmium spp. in the tropical N Atlantic Ocean. Deep-Sea Res I 51:173–203. CrossRefGoogle Scholar
  8. 8.
    Sohm JA, Webb EA, Capone DG (2011) Emerging patterns of marine nitrogen fixation. Nat Rev Microbiol 9(7):499–508. CrossRefPubMedGoogle Scholar
  9. 9.
    Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554. CrossRefPubMedGoogle Scholar
  10. 10.
    Zehr JP, Mellon MT, Zani S (1998) New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Appl Environ Microbiol 64:3444–3450PubMedPubMedCentralGoogle Scholar
  11. 11.
    Kong LL, Jing HM, Kataoka T, Sun J, Liu H (2011) Phylogenetic diversity and spatio-temporal distribution of nitrogenase genes (nifH) in the northern South China Sea. Aquat Microb Ecol 65(1):15–27. CrossRefGoogle Scholar
  12. 12.
    Monteiro FM, Follows MJ, Dutkiewicz S (2010) Distribution of diverse nitrogen fixers in the global ocean. Glob Biogeochem Cycles 24:GB3017. CrossRefGoogle Scholar
  13. 13.
    Cheung SY, Suzuki K, Saito H, Umezawa Y, Xia X, Liu H (2017) Highly heterogeneous diazotroph communities in the Kuroshio current and the Tokara Strait, Japan. PLoS One 12(10):e0186875. CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Shiozaki T, Ijichi M, Kodama T, Takeda S, Furuya K (2014) Heterotrophic bacteria as major nitrogen fixers in the euphotic zone of the Indian Ocean. Glob Biogeochem Cycles 28:1096–1110. CrossRefGoogle Scholar
  15. 15.
    Moisander PH, Serros T, Paerl RW, Beinart RA, Zehr JP (2014) Gammaproteobacterial diazotrophs and nifH gene expression in surface waters of the South Pacific Ocean. ISME J 8(10):1962–1973. CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Bombar D, Paerl RW, Riemann L (2016) Marine non-cyanobacterial diazotrophs: moving beyond molecular detection. Trends Microbiol 24(11):916–927. CrossRefPubMedGoogle Scholar
  17. 17.
    Schott FA, Xie SP, McCreary JP (2009) Indian ocean circulation and climate variability. Rev Geophys 47(1):RG1002. CrossRefGoogle Scholar
  18. 18.
    Wang J, Kan JJ, Zhang XD et al (2017) Archaea dominate the ammonia-oxidizing community in deep-sea sediments of the Eastern Indian Ocean-from the equator to the Bay of Bengal. Front Microbiol 8:1–16. CrossRefGoogle Scholar
  19. 19.
    Singh A, Jani RA, Ramesh R (2010) Spatiotemporal variations of the δ18O-salinity relation in the northern Indian Ocean. Deep-Sea Res I 57(11):1422–1431. CrossRefGoogle Scholar
  20. 20.
    Singh A, Ramesh R (2015) Environmental controls on new and primary production in the northern Indian Ocean. Prog Oceanogr 131(3):138–145. CrossRefGoogle Scholar
  21. 21.
    Lévy M, Shankar D, André JM, Shenoi SSC, Durand F, de Boyer Montégut C (2009) Basin-wide seasonal evolution of the Indian Ocean’s phytoplankton blooms. J Geophys Res Oceans 112:C12014. CrossRefGoogle Scholar
  22. 22.
    Gomes HR, Goes JI, Saino T (2000) Influence of physical processes and freshwater discharge on the seasonality of phytoplankton regime in the Bay of Bengal. Cont Shelf Res 20:313–330. CrossRefGoogle Scholar
  23. 23.
    Kumar SP, Muraleedharan PM, Prasad TG et al (2002) Why is the Bay of Bengal less productive during summer monsoon compared to the Arabian Sea? Geophys Res Lett 29(24):2235–3770. CrossRefGoogle Scholar
  24. 24.
    Madhupratap M, Gauns M, Ramaiah N et al (2003) Biogeochemistry of the Bay of Bengal: physical, chemical and primary productivity characteristics of the central and western Bay of Bengal during summer monsoon. Deep-Sea Res II 50(5):881–896. CrossRefGoogle Scholar
  25. 25.
    Hegde S, Anil AC, Patil JS et al (2008) Influence of environmental settings on the prevalence of Trichodesmium spp. in the Bay of Bengal. Mar Ecol Prog Ser 356(01):93–101. CrossRefGoogle Scholar
  26. 26.
    Gandhi N, Singh A, Prakash S, Ramesh R, Raman M, Sheshshayee MS, Shetye S (2011) First direct measurements of N2 fixation during a Trichodesmium bloom in the eastern Arabian Sea. Glob Biogeochem Cycles 25:GB4014. CrossRefGoogle Scholar
  27. 27.
    Ahmed A, Gauns M, Kurian S (2017) Nitrogen fixation rates in the eastern Arabian Sea. Estuar Coast Shelf Sci 191:74–83. CrossRefGoogle Scholar
  28. 28.
    Bird C, Wyman M (2012) Transcriptionally active heterotrophic diazotrophs are widespread in the upper water column of the Arabian Sea. FEMS Microbiol Ecol 84(1):189–200. CrossRefPubMedGoogle Scholar
  29. 29.
    Kitajima S, Furuya K, Hashihama F, Takeda S, Kanda J (2009) Latitudinal distribution of diazotrophs and their nitrogen fixation in the tropical and subtropical western North Pacific. Limnol Oceanogr 54(2):537–547. CrossRefGoogle Scholar
  30. 30.
    Shiozaki T, Bombar D, Riemann L, Hashihama F, Takeda S, Yamaguchi T, Ehama M, Hamasaki K, Furuya K (2017) Basin scale variability of active diazotrophs and nitrogen fixation in the North Pacific, from the tropics to the subarctic Bering Sea. Glob Biogeochem Cycles 31(6):996–1009. CrossRefGoogle Scholar
  31. 31.
    Church MJ, Mahaffey C, Letelier RM, Lukas R, Zehr JP, Karl DM (2009) Physical forcing of nitrogen fixation and diazotroph community structure in the North Pacific subtropical gyre. Glob Biogeochem Cycles 23:GB2020. CrossRefGoogle Scholar
  32. 32.
    Benavides M, Moisander PH, Daley MC, Bode A, Arístegui J (2016) Longitudinal variability of diazotroph abundances in the subtropical North Atlantic Ocean. J Plankton Res 38(3):662–672. CrossRefGoogle Scholar
  33. 33.
    Goebel NL, Turk KA, Achilles KM, Paerl R, Hewson I, Morrison AE, Montoya JP, Edwards CA, Zehr JP (2010) Abundance and distribution of major groups of diazotrophic cyanobacteria and their potential contribution to N2 fixation in the tropical Atlantic Ocean. Environ Microbiol 12(12):3272–3289. CrossRefPubMedGoogle Scholar
  34. 34.
    Shiozaki T, Nagata T, Ijichi M (2015) Nitrogen fixation and the diazotroph community in the temperate coastal region of the northwestern North Pacific. Biogeosciences 12:4751–4764. CrossRefGoogle Scholar
  35. 35.
    Foster RA, Subramaniam A, Mahaffey C (2007) Influence of the Amazon River plume on distributions of free-living and symbiotic cyanobacteria in the western tropical North Atlantic Ocean. Limnol Oceanogr 52(2):517–532. CrossRefGoogle Scholar
  36. 36.
    . Grasshoff K, Ehrhardt M, Kremling K (1982) Methods of seawater analysis. ISBN (Verlag Chemie), 3– 527, 25,998–26,008Google Scholar
  37. 37.
    Schmidt TM, Delong EF, Pace NR (1991) Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing. J Bacteriol 173:4371–4378. CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Kan JJ, Clingenpeel S, Macur RE et al (2011) Archaea in Yellowstone Lake. ISME J 5(11):1784–1795. CrossRefGoogle Scholar
  39. 39.
    Zhang Y, Yang Q, Ling J et al (2017) Diversity and structure of diazotrophic communities in mangrove rhizosphere, revealed by high-throughput sequencing. Front Microbiol 8(2032).
  40. 40.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Magoč T, Salzberg SL (2010) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. CrossRefGoogle Scholar
  42. 42.
    Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120. CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Kunin V, Engelbrektson A, Ochman H, Hugenholtz P (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12:118–123. CrossRefPubMedGoogle Scholar
  44. 44.
    Huse SM, Huber JA, Morrison HG, Sogin ML, Welch DM (2007) Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 8:R143. CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17(3):377–386. CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Letunic I, Bork P (2011) Interactive tree of life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:475–478. CrossRefGoogle Scholar
  51. 51.
    Zhang Y, Zhao ZH, Sun J (2011) Diversity and distribution of diazotrophic communities in the South China Sea deep basin with mesoscale cyclonic eddy perturbations. FEMS Microbiol Ecol 78(3):417–427. CrossRefPubMedGoogle Scholar
  52. 52.
    R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3–900051–07-0, URL Accessed 31 Oct 2016
  53. 53.
    Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547. CrossRefPubMedGoogle Scholar
  54. 54.
    Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (hill numbers). Methods Ecol Evol 7:1451–1456. CrossRefGoogle Scholar
  55. 55.
    . Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. Marine Laboratory, Plymouth, UK, pp 190Google Scholar
  56. 56.
    ter Braak CJF, Šmilauer P (2002) Canoco for Windows, version 4.5. Biometris-Plant Research International, WageningenGoogle Scholar
  57. 57.
    Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  58. 58.
    Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14(6):927–930. CrossRefGoogle Scholar
  59. 59.
    Schlitzer R (2018) Ocean data view. Accessed 19 May 2018
  60. 60.
    Martínez-Pérez C, Mohr W, Schwedt A, Dürschlag J, Callbeck CM, Schunck H, Dekaezemacker J, Buckner CRT, Lavik G, Fuchs BM, Kuypers MMM (2018) Metabolic versatility of a novel N2-fixing Alphaproteobacterium isolated from a marine oxygen minimum zone. Environ Microbiol 20(2):755–768. CrossRefPubMedGoogle Scholar
  61. 61.
    Riemann L, Farnelid H, Steward GF (2010) Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters. Aquat Microb Ecol 61:235–247. CrossRefGoogle Scholar
  62. 62.
    Farnelid H, Andersson AF, Bertilsson S, al-Soud WA, Hansen LH, Sørensen S, Steward GF, Hagström Å, Riemann L (2011) Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria. PLoS One 6(4):e19223. CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Bentzon-Tilia M, Traving SJ, Mantikci M, Knudsen-Leerbeck H, Hansen JLS, Markager S, Riemann L (2015) Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries. ISME J 9(2):273–285. CrossRefPubMedGoogle Scholar
  64. 64.
    Delmont TO, Quince C, Shaiber A et al (2018) Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes. Nat Microbiol 3:804–813. CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Halm H, Lam P, Ferdelman TG, Lavik G, Dittmar T, LaRoche J, D'Hondt S, Kuypers MMM (2012) Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre. ISME J 6(6):1238–1249. CrossRefPubMedGoogle Scholar
  66. 66.
    Duan YL, Liu L, Han G, Liu H, Yu W, Yang G, Wang H, Wang H, Liu Y, Zahid, Waheed H (2016) Anomalous behaviors of Wyrtki Jets in the equatorial Indian Ocean during 2013. Sci Rep 6:29688. CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Qian G, Wang J, Kan JJ, Zhang X, Xia Z, Zhang X, Miao Y, Sun J (2018) Diversity and distribution of anammox bacteria in water column and sediments of the Eastern Indian Ocean. Int Biodeterior Biodegrad 133:52–62. CrossRefGoogle Scholar
  68. 68.
    Rahav E, Giannetto MJ, Bar-Zeev (2016) Contribution of mono and polysaccharides to heterotrophic N2 fixation at the eastern Mediterranean coastline. Sci Rep 6:27858. CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Moisander PH, Zhang RF, Boyle EA, Hewson I, Montoya JP, Zehr JP (2012) Analogous nutrient limitations in unicellular diazotrophs and Prochlorococcus in the South Pacific Ocean. ISME J 6:733–744. CrossRefPubMedGoogle Scholar
  70. 70.
    Loescher CR, GroβKopf T, Desai FD et al (2014) Facets of diazotroph in the oxygen minimum zone waters off Peru. ISME J 8(11):2180–2192. CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Grand MM, Measures CI, Hatta M, Hiscock WT, Buck CS, Landing WM (2015) Dust deposition in the eastern Indian Ocean: the ocean perspective from Antarctica to the Bay of Bengal. Glob Biogeochem Cycles 29(3):357–374. CrossRefGoogle Scholar
  72. 72.
    Grand MM, Measures CI, Hatta M, Hiscock WT, Landing WM, Morton PL, Buck CS, Barrett PM, Resing JA (2015) Dissolved Fe and Al in the upper 1000 m of the eastern Indian Ocean: a high-resolution transect from the Antarctic margin to the bay of Bengal. Glob Biogeochem Cycles 29(3):375–396. CrossRefGoogle Scholar
  73. 73.
    He Q, Zhan H, Shuai Y (2017) Phytoplankton bloom triggered by an anticyclonic eddy: the combined effect of eddy-Ekman pumping and winter mixing. J Geophys Res-Oceans 122:4886–4901. CrossRefGoogle Scholar
  74. 74.
    Jyothibabu R, Karnan C, Jagadeesan L, Arunpandi N, Pandiarajan RS, Muraleedharan KR, Balachandran KK (2017) Trichodesmium blooms and warm-core ocean surface features in the Arabian Sea and the Bay of Bengal. Mar Pollut Bull 121(1–2):201–215. CrossRefPubMedGoogle Scholar
  75. 75.
    Wu C, Fu FX, Sun J et al (2018) Nitrogen fixation by Trichodesmium and unicellular diazotrophs in the northern South China Sea and the Kuroshio in summer. Sci Rep 8(2415).
  76. 76.
    Cabello AM, Cornejo-Castillo FM, Raho N, Blasco D, Vidal M, Audic S, de Vargas C, Latasa M, Acinas SG, Massana R (2016) Global distribution and vertical patterns of a prymnesiophyte–cyanobacteria obligate symbiosis. ISME J 10(3):693–706. CrossRefPubMedGoogle Scholar
  77. 77.
    Stenegren M, Caputo A, Berg C, Bonnet S, Foster RA (2018) Distribution and drivers of symbiotic and free-living diazotrophic cyanobacteria in the Western Tropical South Pacific. Biogeosciences 15(5):1559–1578. CrossRefGoogle Scholar
  78. 78.
    Cornejo-Castillo FM, Cabello AM, Salazar G, Sánchez-Baracaldo P, Lima-Mendez G, Hingamp P, Alberti A, Sunagawa S, Bork P, de Vargas C, Raes J, Bowler C, Wincker P, Zehr JP, Gasol JM, Massana R, Acinas SG (2016) Cyanobacterial symbionts diverged in the late cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton. Nat Commun 7:11071. CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Turk-Kubo KA, Farnelid HM, Shilova IN, Henke B, Zehr JP (2016) Distinct ecological niches of marine symbiotic N2-fixing cyanobacterium Candidatus atelocyanobacterium thalassa sublineages. J Phycol 53(2):451–461. CrossRefGoogle Scholar
  80. 80.
    Fu FX, Yu E, Garcia NS, Gale J, Luo Y, Webb EA, Hutchins DA (2014) Differing responses of marine N2-fixers to warming and consequences for future diazotroph community structure. Aquat Microb Ecol 72:33–46. CrossRefGoogle Scholar
  81. 81.
    Heiniger EK, Oda Y, Samanta SK, Harwood CS (2012) How posttranslational modification of nitrogenase is circumvented in Rhodopseudomonas palustris strains that produce hydrogen gas constitutively. Appl Environ Microbiol 78:1023–1032. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Marine Science and TechnologyShandong UniversityQingdaoChina
  2. 2.Microbiology DivisionStroud Water Research CenterAvondaleUSA
  3. 3.Tianjin Key Laboratory of Marine Resources and ChemistryTianjin University of Science and TechnologyTianjinChina
  4. 4.Research Centre for Indian Ocean EcosystemTianjin University of science and TechnologyTianjinChina
  5. 5.College of Marine & Environmental SciencesTianjin University of Science and TechnologyTianjinPeople’s Republic of China

Personalised recommendations