Skip to main content
Log in

Variation of bacterial community associated with Phaeodactylum tricornutum in response to different inorganic nitrogen concentrations

  • Published:
Acta Oceanologica Sinica Aims and scope Submit manuscript

Abstract

Specific bacterial communities interact with phytoplankton in laboratory algal cultures. These communities influence phytoplankton physiology and metabolism by transforming and exchanging phytoplankton-derived organic matter. Functional bacterial groups may participate in various critical nutrients fluxes within these associations, including nitrogen (N) metabolism. However, it is unclear how bacterial communities and the associated algae respond to changes of phycosphere N conditions. This response may have far-reaching implications for global nutrient cycling, algal bloom formation, and ecosystem function. Here, we identified changes in the bacterial communities associated with Phaeodactylum tricornutum when co-cultured with different forms and concentrations of N based on the Illumina HiSeq sequencing of 16S rRNA amplicons. Phylogenetic analysis identified Proteobacteria and Bacteroidetes as the dominant phyla, accounting for 99.5% of all sequences. Importantly, bacterial abundance and community structure were more affected by algal abundance than by the form or concentration of inorganic N. The relative abundance of three gammaproteobacterial genera (Marinobacter, Algiphilus and Methylophaga) markedly increased in N-deficient cultures. Thus, some bacterial groups may play a role in the regulation of N metabolism when co-cultured with P. tricornutum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alavi M, Miller T, Erlandson K, et al. 2001. Bacterial community associated with Pfiesteria-like dinoflagellate cultures. Environmental Microbiology, 3(6): 380–396

    Article  Google Scholar 

  • Amin S A, Green D H, Hart M C, et al. 2009. Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. Proceedings of the National Academy of Sciences of the United States of America, 106(40): 17071–17076

    Article  Google Scholar 

  • Amin S A, Hmelo L R, Van Tol H M, et al. 2015. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature, 522(7554): 98–101

    Article  Google Scholar 

  • Amin S A, Parker M S, Armbrust E V. 2012. Interactions between diatoms and bacteria. Microbiology and Molecular Biology Reviews, 76(3): 667–684

    Article  Google Scholar 

  • Balvanera P, Pfisterer A B, Buchmann N, et al. 2006. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters, 9(10): 1146–1156

    Article  Google Scholar 

  • Behringer G, Ochsenkühn M A, Fei Cong, et al. 2018. Bacterial communities of diatoms display strong conservation across strains and time. Frontiers in Microbiology, 9: 659

    Article  Google Scholar 

  • Bell W, Mitchell R. 1972. Chemotactic and growth responses of marine bacteria to algal extracellular products. The Biological Bulletin, 143(2): 265–277

    Article  Google Scholar 

  • Bell W H. 1984. Bacterial adaptation to low-nutrient conditions as studied with algal extracellular products. Microbial Ecology, 10(3): 217–230

    Article  Google Scholar 

  • Bolch C J S, Bejoy T A, Green D H. 2017. Bacterial associates modify growth dynamics of the dinoflagellate Gymnodinium catenatum. Frontiers in Microbiology, 8: 670

    Article  Google Scholar 

  • Borcard D, Gillet F, Legendre P. 2011. Numerical Ecology with R. New York: Springer, 115–151

    Book  Google Scholar 

  • Bowler C, Allen A E, Badger J H, et al. 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature, 456(7219): 239–244

    Article  Google Scholar 

  • Buchan A, Collier L S, Neidle E L, et al. 2000. Key aromatic-ringcleaving enzyme, protocatechuate 3,4-Dioxygenase, in the ecologically important marine Roseobacter Lineage. Applied and Environmental Microbiology, 66(11): 4662–4672

    Article  Google Scholar 

  • Buchan A, LeCleir G R, Gulvik C A, et al. 2014. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nature Reviews Microbiology, 12(10): 686–698

    Article  Google Scholar 

  • Capone D G, Bronk D A, Mulholland M R, et al. 2008. Nitrogen in the Marine Environment. 2nd ed. San Diego: Academic Press, 757

    Google Scholar 

  • Caporaso J G, Kuczynski J, Stombaugh J, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5): 335–336

    Article  Google Scholar 

  • Caporaso J G, Lauber C L, Walters W A, et al. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America, 108(Suppl 1): 4516–4522

    Article  Google Scholar 

  • Casciotti K L. 2016. Nitrogen and oxygen isotopic studies of the marine nitrogen cycle. Annual Review of Marine Science, 8: 379–407

    Article  Google Scholar 

  • Chapin III F S I, Zavaleta E S, Eviner V T, et al. 2000. Consequences of changing biodiversity. Nature, 405(6783): 234–242

    Article  Google Scholar 

  • Chiu H C, Levy R, Borenstein E. 2014. Emergent biosynthetic capacity in simple microbial communities. PLoS Computational Biology, 10(7): e1003695

    Article  Google Scholar 

  • Croft M T, Lawrence A D, Raux-Deery E, et al. 2005. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature, 438(7064): 90–93

    Article  Google Scholar 

  • de-Bashan L E, Antoun H, Bashan Y. 2008. Involvement of indole-3-acetic acid produced by the growth-promoting bacterium Azospirillum spp. in promoting growth of Chlorella vulgaris. Journal of Phycology, 44(4): 938–947

    Article  Google Scholar 

  • De La Haba R R, Sánchez-Porro C, Marquez M C, et al. 2011. Taxonomy of halophiles. In: Horikoshi K, ed. Extremophiles Handbook. Tokyo: Springer, 255–265

    Google Scholar 

  • De Martino A, Bartual A, Willis A, et al. 2011. Physiological and molecular evidence that environmental changes elicit morphological interconversion in the model diatom Phaeodactylum tricornutum. Protist, 162(3): 462–481

    Article  Google Scholar 

  • Donald D B, Bogard M J, Finlay K, et al. 2011. Comparative effects of urea, ammonium, and nitrate on phytoplankton abundance, community composition, and toxicity in hypereutrophic freshwaters. Limnology and Oceanography, 56(6): 2161–2175

    Article  Google Scholar 

  • Edgar R C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10): 996–998

    Article  Google Scholar 

  • Edgar R C, Haas B J, Clemente J C, et al. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16): 2194–2200

    Article  Google Scholar 

  • Foster R A, Kuypers M M M, Vagner T, et al. 2011. Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. ISME Journal, 5(9): 1484–1493

    Article  Google Scholar 

  • Fowler D, Coyle M, Skiba U, et al. 2013. The global nitrogen cycle in the twenty-first century. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1621): 20130164

    Article  Google Scholar 

  • Gauthier M J, Lafay B, Christen R, et al. 1992. Marinobacter hydrocarbonoclasticus gen. nov., sp. nov., a new, extremely halotolerant, hydrocarbon-degrading marine bacterium. International Journal of Systematic and Evolutionary Microbiology, 42(4): 568–576

    Google Scholar 

  • González J M, Kiene R P, Moran M A. 1999. Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class Proteobacteria. Applied and Environmental Microbiology, 65(9): 3810–3819

    Google Scholar 

  • Green D H, Echavarri-Bravo V, Brennan D, et al. 2015. Bacterial diversity associated with the coccolithophorid algae Emiliania huxleyi and Coccolithus pelagicus f. braarudii. BioMed Research International, 2015: 194540

    Google Scholar 

  • Green D H, Hart M C, Blackburn S I, et al. 2010. Bacterial diversity of Gymnodinium catenatum and its relationship to dinoflagellate toxicity. Aquatic Microbial Ecology, 61(1): 73–87

    Article  Google Scholar 

  • Green D H, Llewellyn L E, Negri A P, et al. 2004. Phylogenetic and functional diversity of the cultivable bacterial community associated with the paralytic shellfish poisoning dinoflagellate Gymnodinium catenatum. FEMS Microbiology Ecology, 47(3): 345–357

    Article  Google Scholar 

  • Grossart H P, Levold F, Allgaier M, et al. 2010. Marine diatom species harbour distinct bacterial communities. Environmental Microbiology, 7(6): 860–873

    Article  Google Scholar 

  • Guillard R R L. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Smith W L, Chanley M H, ed. Culture of Marine Invertebrate Animals. Boston, MA: Springer, 29–60

    Chapter  Google Scholar 

  • Guillard R R L, Ryther J H. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Canadian Journal of Microbiology, 8(2): 229–239

    Article  Google Scholar 

  • Gutierrez T, Green D H, Whitman W B, et al. 2012. Algiphilus aromaticivorans gen. nov., sp. nov., an aromatic hydrocarbon-degrading bacterium isolated from a culture of the marine dinoflagellate Lingulodinium polyedrum, and proposal of Algiphilaceae fam. nov.. International Journal of Systematic and Evolutionary Microbiology, 62(11): 2743–2749

    Article  Google Scholar 

  • Haas B J, Gevers D, Earl A M, et al. 2011. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21(3): 494–504

    Article  Google Scholar 

  • Haines K C, Guillard R R L. 1974. Growth of vitamin B12-requiring marine diatoms in mixed laboratory cultures with vitamin B12-producing marine bacteria. Journal of Phycology, 10(3): 245–252

    Google Scholar 

  • Hatton A D, Shenoy D M, Hart M C, et al. 2012. Metabolism of DMSP, DMS and DMSO by the cultivable bacterial community associated with the DMSP-producing dinoflagellate Scrippsiella trochoidea. Biogeochemistry, 110(1–3): 131–146

    Article  Google Scholar 

  • Jasti S, Sieracki M E, Poulton N J, et al. 2005. Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Applied and Environmental Microbiology, 71(7): 3483–3494

    Article  Google Scholar 

  • Kaczmarska I, Ehrman J M, Bates E S S, et al. 2005. Diversity and distribution of epibiotic bacteria on Pseudo-nitzschia multiseries (Bacillariophyceae) in culture, and comparison with those on diatoms in native seawater. Harmful Algae, 4(4): 725–741

    Article  Google Scholar 

  • Kuo R C, Lin Senjie. 2013. Ectobiotic and endobiotic bacteria associated with Eutreptiella sp. isolated from Long Island Sound. Protist, 164(1): 60–74

    Article  Google Scholar 

  • Langille M G I, Zaneveld J, Caporaso J G, et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology, 31(9): 814–821

    Article  Google Scholar 

  • Li Yang, Wang Zhen, Lin Xuezheng. 2016. Microbial community structure of Arctic seawater as revealed by pyrosequencing. Acta Oceanologica Sinica, 35(6): 78–84

    Article  Google Scholar 

  • Little A E F, Robinson C J, Peterson S B, et al. 2008. Rules of engagement: interspecies interactions that regulate microbial communities. Annual Review of Microbiology, 62: 375–401

    Article  Google Scholar 

  • Liu Lemian, Yang Jun, Lv Hong, et al. 2015. Phytoplankton communities exhibit a stronger response to environmental changes than bacterioplankton in three subtropical reservoirs. Environmental Science & Technology, 49(18): 10850–10858

    Article  Google Scholar 

  • Løvdal T, Eichner C, Grossart H P, et al. 2008. Competition for inorganic and organic forms of nitrogen and phosphorous between phytoplankton and bacteria during an Emiliania huxleyi spring bloom. Biogeosciences, 5(2): 371–383

    Article  Google Scholar 

  • Lupette J, Lami R, Krasovec M, et al. 2016. Marinobacter dominates the bacterial community of the Ostreococcus tauri phycosphere in culture. Frontiers in Microbiology, 7: 1414

    Article  Google Scholar 

  • Ma Yuexin, Tao Wei, Liu Changfa, et al. 2017. Response of microbial biomass and bacterial community composition to fertilization in a salt marsh in China. Acta Oceanologica Sinica, 36(6): 80–88

    Article  Google Scholar 

  • Magoč T, Salzberg S L. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21): 2957–2963

    Article  Google Scholar 

  • Maheswari U, Jabbari K, Petit J L, et al. 2010. Digital expression profiling of novel diatom transcripts provides insight into their biological functions. Genome Biology, 11(8): R85

    Article  Google Scholar 

  • Martens-Habbena W, Berube P M, Urakawa H, et al. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature, 461(7266): 976–979

    Article  Google Scholar 

  • Maruyama A, Maeda M, Simidu U. 1986. Occurrence of plant hormone (cytokinin)-producing bacteria in the sea. Journal of Applied Bacteriology, 61(6): 569–574

    Article  Google Scholar 

  • Mayali X, Azam F. 2004. Algicidal bacteria in the sea and their impact on algal blooms. Journal of Eukaryotic Microbiology, 51(2): 139–144

    Article  Google Scholar 

  • Miller T R, Belas R. 2004. Dimethylsulfoniopropionate metabolism by Pfiesteria-associated Roseobacter spp.. Applied and Environmental Microbiology, 70(6): 3383–3391

    Article  Google Scholar 

  • Paerl H W, Dyble J, Moisander P H, et al. 2003. Microbial indicators of aquatic ecosystem change: current applications to eutrophication studies. FEMS Microbiology Ecology, 46(3): 233–246

    Article  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, et al. 2013. The SILVA ribosomal RNA gene database project: improved data processing and webbased tools. Nucleic Acids Research, 41(D1): D590–D596

    Google Scholar 

  • Ramanan R, Kim B H, Cho D H, et al. 2016. Algae-bacteria interactions: Evolution, ecology and emerging applications. Biotechnology Advances, 34(1): 14–29

    Article  Google Scholar 

  • Ramirez K S, Lauber C L, Knight R, et al. 2010. Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology, 91(12): 3463–3470

    Article  Google Scholar 

  • Risgaard-Petersen N, Nicolaisen M H, Revsbech N P, et al. 2004. Competition between ammonia-oxidizing bacteria and benthic microalgae. Applied and Environmental Microbiology, 70(9): 5528–5537

    Article  Google Scholar 

  • Rooney-Varga J N, Giewat M W, Savin M C, et al. 2005. Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microbial Ecology, 49(1): 163–175

    Article  Google Scholar 

  • Sapp M, Wichels A, Wiltshire K H, et al. 2007. Bacterial community dynamics during the winter-spring transition in the North Sea. FEMS Microbiology Ecology, 59(3): 622–637

    Article  Google Scholar 

  • Sasaki K, Ikeda S, Ohkubo T, et al. 2013. Effects of plant genotype and nitrogen level on bacterial communities in rice shoots and roots. Microbes and Environments, 28(3): 391–395

    Article  Google Scholar 

  • Schäfer H, Abbas B, Witte H, et al. 2002. Genetic diversity of ‘satellite’ bacteria present in cultures of marine diatoms. FEMS Microbiology Ecology, 42(1): 25–35

    Google Scholar 

  • Segata N, Izard J, Waldron L, et al. 2011. Metagenomic biomarker discovery and explanation. Genome Biology, 12(6): R60

    Book  Google Scholar 

  • Seymour J R, Amin S A, Raina J B, et al. 2017. Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nature Microbiology, 2: 17065

    Article  Google Scholar 

  • Seibold A, Wichels A, Schütt C. 2001. Diversity of endocytic bacteria in the dinoflagellate Noctiluca scintillans. Aquatic Microbial Ecology, 25(3): 229–235

    Article  Google Scholar 

  • Villeneuve C, Martineau C, Mauffrey F, et al. 2013. Methylophaga nitratireducenticrescens sp. nov. and Methylophaga frappieri sp. nov., isolated from the biofilm of the methanol-fed denitrification system treating the seawater at the Montreal Biodome. International Journal of Systematic and Evolutionary Microbiology, 63(6): 2216–2222

    Article  Google Scholar 

  • Wang Qiong, Garrity G M, Tiedje J M, et al. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5261–5267

    Article  Google Scholar 

  • Wang Xin, Li Zhijiang, Su Jianqiang, et al. 2010. Lysis of a red-tide causing alga, Alexandrium tamarense, caused by bacteria from its phycosphere. Biological Control, 52(2): 123–130

    Article  Google Scholar 

  • Wemheuer B, Güllert S, Billerbeck S, et al. 2014. Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. FEMS Microbiology Ecology, 87(2): 378–389

    Article  Google Scholar 

  • Yang Caiyun, Li Yi, Zhou B, et al. 2015. Illumina sequencing-based analysis of free-living bacterial community dynamics during an Akashiwo sanguine bloom in Xiamen sea, China. Scientific Reports, 5: 8476

    Article  Google Scholar 

  • Zehr J P, Kudela R M. 2010. Nitrogen cycle of the open ocean: from genes to ecosystems. Annual Review of Marine Science, 3: 197–225

    Article  Google Scholar 

  • Zehr J P, Ward B B. 2002. Nitrogen cycling in the ocean: new perspectives on processes and paradigms. Applied and Environmental Microbiology, 68(3): 1015–1024

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jianfeng Feng or Lin Zhu.

Additional information

Foundation item: The National Natural Science Foundation of China (NSFC) under contract No. 31470536; the National Key Research and Development Program of China under contract No. 2018YFC1406403.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shi, F., Wei, X., Feng, J. et al. Variation of bacterial community associated with Phaeodactylum tricornutum in response to different inorganic nitrogen concentrations. Acta Oceanol. Sin. 37, 118–128 (2018). https://doi.org/10.1007/s13131-018-1272-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13131-018-1272-7

Key words

Navigation