Phaeocystis is a cosmopolitan, bloom-forming phytoplankton genus that contributes significantly to global carbon and sulfur cycles. During blooms, Phaeocystis species produce large carbon-rich colonies, creating a unique interface for bacterial interactions. While bacteria are known to interact with phytoplankton—e.g., they promote growth by producing phytohormones and vitamins—such interactions have not been shown for Phaeocystis. Therefore, we investigated the composition and function of P. globosa microbiomes. Specifically, we tested whether microbiome compositions are consistent across individual colonies from four P. globosa strains, whether similar microbiomes are re-recruited after antibiotic treatment, and how microbiomes affect P. globosa growth under limiting conditions. Results illuminated a core colonial P. globosa microbiome—including bacteria from the orders Alteromonadales, Burkholderiales, and Rhizobiales—that was re-recruited after microbiome disruption. Consistent microbiome composition and recruitment is indicative that P. globosa microbiomes are stable-state systems undergoing deterministic community assembly and suggests there are specific, beneficial interactions between Phaeocystis and bacteria. Growth experiments with axenic and nonaxenic cultures demonstrated that microbiomes allowed continued growth when B-vitamins were withheld, but that microbiomes accelerated culture collapse when nitrogen was withheld. In sum, this study reveals symbiotic and opportunistic interactions between Phaeocystis colonies and microbiome bacteria that could influence large-scale phytoplankton bloom dynamics and biogeochemical cycles.
This is a preview of subscription content, access via your institution
Subscribe to Journal
Get full journal access for 1 year
only $9.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
All sequencing data generated for this manuscript is available from the NCBI SRA under accession PRJN779092.
Moran MA, Kujawinski EB, Stubbins A, Fatland R, Aluwihare LI, Buchan A, et al. Deciphering ocean carbon in a changing world. Proc Natl Acad Sci USA 2016;113:3143–51.
Seymour JR, Amin SA, Raina J-B, Stocker R Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat Microbiol. 2017;2:17065.
Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science. 2011;332:1097–1100.
Cirri E, Pohnert G. Algae-bacteria interactions that balance the planktonic microbiome. N. Phytol. 2019;223:100–6.
Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT, Heal KR, et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature. 2015;522:98–101.
Grant MAA, Kazamia E, Cicuta P, Smith AG. Direct exchange of vitamin B12 is demonstrated by modelling the growth dynamics of algal-bacterial cocultures. ISME J. 2014;8:1418–27.
Bertrand EM, McCrow JP, Moustafa A, Zheng H, McQuaid JB, Delmont TO, et al. Phytoplankton-bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge. Proc Natl Acad Sci USA 2015;112:9938–43.
Durham BP, Sharma S, Luo H, Smith CB, Amin SA, Bender SJ, et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proc Natl Acad Sci USA 2015;112:453–7.
Suleiman M, Zecher K, Yücel O, Jagmann N, Philipp B. Interkingdom cross-feeding of ammonium from marine methylamine-degrading bacteria to the diatom Phaeodactylum tricornutum. Appl Environ Microbiol. 2016;82:7113–22.
Seyedsayamdost MR, Case RJ, Kolter R, Clardy J. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem. 2011;3:331–5.
Ratnarajah L, Blain S, Boyd PW, Fourquez M, Obernosterer I, Tagliabue A. Resource colimitation drives competition between phytoplankton and bacteria in the Southern Ocean. Geophys Res Lett. 2021;48:e2020GL088369.
Løvdal T, Eichner C, Grossart H-P, Carbonnel V, Chou L, Martin-Jézéquel V, et al. Competition for inorganic and organic forms of nitrogen and phosphorous between phytoplankton and bacteria during an Emiliania huxleyi spring bloom. Biogeosciences. 2008;5:371–83.
Arrigo KR, Robinson DH, Worthen DL, Dunbar RB, DiTullio GR, VanWoert M, et al. Phytoplankton community structure and the drawdown of nutrients and CO2 in the Southern Ocean. Science. 1999;283:365–7.
Geider R, La Roche J. Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur J Phycol. 2002;37:1–17.
Smayda TJ. Normal and accelerated sinking of phytoplankton in the sea. Mar Geol. 1971;11:105–22.
Amin SA, Parker MS, Armbrust EV. Interactions between diatoms and bacteria. Microbiol Mol Biol Rev. 2012;76:667–84.
Tréguer P, Bowler C, Moriceau B, Dutkiewicz S, Gehlen M, Aumont O, et al. Influence of diatom diversity on the ocean biological carbon pump. Nat Geosci. 2018;11:27–37.
Ferrer-González FX, Widner B, Holderman NR, Glushka J, Edison AS, Kujawinski EB, et al. Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy. ISME J. 2021;15:762–73.
Mönnich J, Tebben J, Bergemann J, Case R, Wohlrab S, Harder T. Niche-based assembly of bacterial consortia on the diatom Thalassiosira rotula is stable and reproducible. ISME J. 2020;14:1614–25.
Shibl AA, Isaac A, Ochsenkühn MA, Cárdenas A, Fei C, Behringer G, et al. Diatom modulation of select bacteria through use of two unique secondary metabolites. Proc Natl Acad Sci USA 2020;117:27445–55.
Schoemann V, Becquevort S, Stefels J, Rousseau V, Lancelot C. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res. 2005;53:43–66.
Peperzak L, Colijn F, Gieskes WWC, Peeters JCH. Development of the diatom-Phaeocystis spring bloom in the Dutch coastal zone of the North Sea: the silicon depletion versus the daily irradiance threshold hypothesis. J Plankton Res. 1998;20:517–37.
Hai D-N, Lam N-N, Dippner JW. Development of Phaeocystis globosa blooms in the upwelling waters of the south central coast of Viet Nam. J Mar Syst. 2010;83:253–61.
Wang X, Song H, Wang Y, Chen N. Research on the biology and ecology of the harmful algal bloom species Phaeocystis globosa in China: Progresses in the last 20 years. Harmful Algae. 2021;107:102057.
Jiang M, Borkman DG, Scott Libby P, Townsend DW, Zhou M. Nutrient input and the competition between Phaeocystis pouchetii and diatoms in Massachusetts Bay spring bloom. J Mar Syst. 2014;134:29–44.
Nissen C, Vogt M. Factors controlling the competition between Phaeocystis and diatoms in the Southern Ocean and implications for carbon export fluxes. Biogeosciences. 2021;18:251–83.
Mars Brisbin M, Mitarai S. Differential gene expression supports a resource-intensive, defensive role for colony production in the bloom-forming haptophyte, Phaeocystis globosa. J Eukaryot Microbiol. 2019;66:788–801.
Zhu Z, Meng R, Smith WO Jr, Doan-Nhu H, Nguyen-Ngoc L, Jiang X. Bacterial composition associated with giant colonies of the harmful algal species Phaeocystis globosa. Front Microbiol. 2021;12:737484.
Delmont TO, Hammar KM, Ducklow HW, Yager PL, Post AF. Phaeocystis antarctica blooms strongly influence bacterial community structures in the Amundsen Sea polynya. Front Microbiol. 2014;5:646.
Verity PG, Whipple SJ, Nejstgaard JC, Alderkamp A-C. Colony size, cell number, carbon and nitrogen contents of Phaeocystis pouchetii from western Norway. J Plankton Res. 2007;29:359–67.
Alderkamp A-C, Buma AGJ, van Rijssel M. The carbohydrates of Phaeocystis and their degradation in the microbial food web. Biogeochemistry. 2007;83:99–118.
Smriga S, Fernandez VI, Mitchell JG, Stocker R. Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria. Proc Natl Acad Sci USA 2016;113:1576–81.
Mühlenbruch M, Grossart H-P, Eigemann F, Voss M. Mini-review: Phytoplankton-derived polysaccharides in the marine environment and their interactions with heterotrophic bacteria. Environ Microbiol. 2018;20:2671–85.
Raina J-B, Fernandez V, Lambert B, Stocker R, Seymour JR. The role of microbial motility and chemotaxis in symbiosis. Nat Rev Microbiol. 2019;17:284–94.
Solomon CM, Lessard EJ, Keil RG, Foy MS. Characterization of extracellular polymers of Phaeocystis globosa and P. antarctica. Mar Ecol Prog Ser. 2003;250:81–89.
Shen P, Qi Y, Wang Y, Huang L. Phaeocystis globosa Scherffel, a harmful microalga, and its production of dimethylsulfoniopropionate. Chin J Oceano Limnol. 2011;29:869–73.
Louca S, Polz MF, Mazel F, Albright MBN, Huber JA, O’Connor MI, et al. Function and functional redundancy in microbial systems. Nat Ecol Evol. 2018;2:936–43.
Wang J, Bouwman AF, Liu X, Beusen AHW, Van Dingenen R, Dentener F, et al. Harmful algal blooms in chinese coastal waters will persist due to perturbed nutrient ratios. Environ Sci Technol Lett. 2021;8:276–84.
Foster RA, Kuypers MMM, Vagner T, Paerl RW, Musat N, Zehr JP. Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. ISME J. 2011;5:1484–93.
Helliwell KE. The roles of B vitamins in phytoplankton nutrition: new perspectives and prospects. N. Phytol. 2017;216:62–68.
Bertrand EM, Saito MA, Rose JM, Riesselman CR, Lohan MC, Noble AE, et al. Vitamin B12 and iron colimitation of phytoplankton growth in the Ross Sea. Limnol Oceanogr. 2007;52:1079–93.
Tang YZ, Koch F, Gobler CJ. Most harmful algal bloom species are vitamin B1 and B12 auxotrophs. Proc Natl Acad Sci USA 2010;107:20756–61.
Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature. 2005;438:90–93.
Guillard RRL, Hargraves PE. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia. 1993;32:234–6.
Hamilton PB, Lefebvre KE, Bull RD. Single cell PCR amplification of diatoms using fresh and preserved samples. Front Microbiol. 2015;6:1084.
dos Reis MC, Romac S, Le Gall F, Marie D, Frada MJ, Koplovitz G, et al. Exploring the phycosphere of Emiliania huxleyi: from bloom dynamics to microbiome assembly experiments. bioRxiv 2022;02;21:481256.
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Glo FO, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–6.
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome. 2018;6:90.
R Core Team. R: A language and environment for statistical computing. 2018. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Mcmurdie PJ, Holmes S phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 2013;8:e61217.
Gloor GB, Macklaim JM, Pawlowsky-Glahn V, Egozcue JJ. Microbiome datasets are compositional: and this is not optional. Front Microbiol. 2017;8:2224.
Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. R package version. 2019;2:5–4.
Ares Á, Brisbin MM, Sato KN, Martín JP, Iinuma Y, Mitarai S. Extreme storms cause rapid but short-lived shifts in nearshore subtropical bacterial communities. Environ Microbiol. 2020;22:4571–88.
Radwan SSA, Al-Mailem DM, Kansour MK. Gelatinizing oil in water and its removal via bacteria inhabiting the gels. Sci Rep. 2017;7:13975.
Behringer G, Ochsenkühn MA, Fei C, Fanning J, Koester JA, Amin SA. Bacterial communities of diatoms display strong conservation across strains and time. Front Microbiol. 2018;9:659.
Glaeser SP, Imani J, Alabid I, Guo H, Kumar N, Kämpfer P, et al. Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica. ISME J. 2016;10:871–84.
Chakraborty U, Chakraborty BN, Dey PL, Chakraborty AP, Sarkar J. Biochemical responses of wheat plants primed with Ochrobactrum pseudogrignonense and subjected to salinity stress. Agric Res. 2019;8:427–40.
Johnson WM, Alexander H, Bier RL, Miller DR, Muscarella ME, Pitz KJ, et al. Auxotrophic interactions: a stabilizing attribute of aquatic microbial communities? FEMS Microbiol Ecol. 2020;96;11:fiaa115.
Ajani PA, Kahlke T, Siboni N, Carney R, Murray SA, Seymour JR. The Microbiome of the cosmopolitan diatom Leptocylindrus reveals significant spatial and temporal variability. Front Microbiol. 2018;9:2758.
Connor EF, McCoy ED. The statistics and biology of the species-area relationship. Am Nat. 1979;113:791–833.
Hamm CE, Simson DA, Merkel R, Smetacek V. Colonies of Phaeocystis globosa are protected by a thin but tough skin. Mar Ecol Prog Ser. 1999;187:101–11.
Geddes BA, Paramasivan P, Joffrin A, Thompson AL, Christensen K, Jorrin B, et al. Engineering transkingdom signalling in plants to control gene expression in rhizosphere bacteria. Nat Commun. 2019;10:3430.
Sieburth JM. Acrylic acid, an‘ antibiotic’ principle in Phaeocystis blooms in Antarctic waters. Science. 1960;132:676–7.
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinform. 2009;10:421.
Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res. 2016;44:D67–72.
López-Pérez M, Gonzaga A, Martin-Cuadrado A-B, Onyshchenko O, Ghavidel A, Ghai R, et al. Genomes of surface isolates of Alteromonas macleodii: the life of a widespread marine opportunistic copiotroph. Sci Rep. 2012;2:696.
Diner RE, Schwenck SM, McCrow JP, Zheng H, Allen AE. Genetic manipulation of competition for nitrate between heterotrophic bacteria and diatoms. Front Microbiol. 2016;7:880.
Monteiro RA, Balsanelli E, Wassem R, Marin AM, Brusamarello-Santos LCC, Schmidt MA, et al. Herbaspirillum-plant interactions: microscopical, histological and molecular aspects. Plant Soil. 2012;356:175–96.
Bastián F, Cohen A, Piccoli P, Luna V, Baraldi R. Production of indole-3-acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically-defined culture media. Plant Growth Regul. 1998;24:7–11.
Gyaneshwar P, James EK, Reddy PM. Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium‐tolerant rice varieties. N. Phytol. 2002;154:131–45.
Guo H, Yang Y, Liu K, Xu W, Gao J, Duan H, et al. Comparative genomic analysis of Delftia tsuruhatensis MTQ3 and the identification of functional NRPS genes for siderophore production. Biomed Res Int. 2016;2016:3687619.
Vásquez-Piñeros MA, Martínez-Lavanchy PM, Jehmlich N, Pieper DH, Rincón CA, Harms H, et al. Delftia sp. LCW, a strain isolated from a constructed wetland shows novel properties for dimethylphenol isomers degradation. BMC Microbiol. 2018;18:108.
Riegman R, Noordeloos AAM, Cadée GC. Phaeocystis blooms and eutrophication of the continental coastal zones of the North Sea. Mar Biol. 1992;112:479–84.
Sañudo-Wilhelmy SA, Cutter LS, Durazo R, Smail EA, Gómez-Consarnau L, Webb EA, et al. Multiple B-vitamin depletion in large areas of the coastal ocean. Proc Natl Acad Sci USA 2012;109:14041–5.
Gobler CJ, Norman C, Panzeca C, Taylor GT, Sañudo-Wilhelmy SA. Effect of B-vitamins (B1, B12) and inorganic nutrients on algal bloom dynamics in a coastal ecosystem. Aquat Micro Ecol. 2007;49:181–94.
Gómez-Consarnau L, Sachdeva R, Gifford SM, Cutter LS, Fuhrman JA, Sañudo-Wilhelmy SA, et al. Mosaic patterns of B-vitamin synthesis and utilization in a natural marine microbial community. Environ Microbiol. 2018;20:2809–23.
Bertrand EM, Saito MA, Jeon YJ, Neilan BA. Vitamin B12 biosynthesis gene diversity in the Ross Sea: the identification of a new group of putative polar B12 biosynthesizers. Environ Microbiol. 2011;13:1285–98.
Research was funded by the Marine Biophysics Unit of the Okinawa Institute of Science and Technology (OIST) Graduate University. MMB was supported by an OIST Junior Research Fellowship, a Postdoctoral Scholarship granted by Woods Hole Oceanographic Institution, and a Simons Foundation Postdoctoral Fellowship in Marine Microbiology (award # 874439). We thank the captain and crew of the Okinawa Prefectural Fisheries and Ocean Research Center ship Tonan Maru for collecting seawater from the East China Sea for the culture of the Kuroshio strain of Phaeocystis globosa. We further thank Kazumi Inoha for coordinating seawater sampling on the Tonan Maru. Dawn Moran provided valuable advice for treating phytoplankton cultures with antibiotics. The OIST DNA sequencing section (Onna, Okinawa, Japan) performed the sequencing for this project.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Mars Brisbin, M., Mitarai, S., Saito, M.A. et al. Microbiomes of bloom-forming Phaeocystis algae are stable and consistently recruited, with both symbiotic and opportunistic modes. ISME J 16, 2255–2264 (2022). https://doi.org/10.1038/s41396-022-01263-2