Colonies of the N2-fixing cyanobacterium Trichodesmium spp. constitute a consortium with multiple microorganisms that collectively exert ecosystem-level influence on marine carbon and nitrogen cycling, shunting newly fixed nitrogen to low nitrogen systems, and exporting both carbon and nitrogen to the deep sea. Here we identify a seasonally recurrent association between puff colonies and amoebae through a two-year survey involving over 10 000 Trichodesmium colonies in the Red Sea. This association was most commonly found in near-shore populations during spring. Microscopic observations revealed consistent amoebae morphology throughout the study, and both morphological characteristics and 18S rRNA gene sequencing suggested that these amoebae are likely to belong to the species Trichosphaerium micrum, an amoeba that forms a CaCO3 shell. Co-cultures of Trichosphaerium micrum and Trichodesmium grown in the laboratory suggest that the amoebae feed on heterotrophic bacteria and not Trichodesmium, which adds a consumer dynamic to the complex microbial interactions within these colonies. Sinking experiments with fresh colonies indicated that the presence of the CaCO3-shelled amoebae decreased colony buoyancy. As such, this novel association may accelerate Trichodesmium sinking rates and facilitate carbon and nitrogen export to the deep ocean. Amoebae have previously been identified in Trichodesmium colonies in the western North Atlantic (Bermuda and Barbados), suggesting that this type of association may be widespread. This association may add a new critical facet to the microbial interactions underpinning carbon and nitrogen fixation and fate in the present and future ocean.

Biology and Paleo Environment Lamont Doherty Earth Observatory of Columbia University 61 Route 9W Palisades NY 10964 United States

CentreAlgatech Institute of Microbiology of the Czech Academy of Sciences Novohradská 237 Třeboň 37901 Czech Republic

Department of Earth and Environmental Sciences Columbia University 1200 Amsterdam Avenue New York NY 10027 United States

Friedrich Alexander University Erlangen Nuernberg Department Geographie und Geowissenschaften Erlangen 91054 GeoZentrum Nordbayern Schlossgarten 5 Germany

Israel Limnology and Oceanography Research Tel Shikmona P O B 8030 Haifa 3108000 Israel

The Fredy and Nadine Herrmann Institute of Earth Sciences Hebrew University of Jerusalem The Edmond J Safra Campus Jerusalem 9190401 Israel

The Interuniversity Institute for Marine Sciences in Eilat Coral Beach P O B 469 Eilat 8810302 Israel

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Moore CM, Mills MM, Arrigo KRet al. . Processes and patterns of oceanic nutrient limitation. Nat Geosci 2013;6:701–10. 10.1038/ngeo1765 DOI

Mahaffey C, Michaels AF, Capone DG. The conundrum of marine N2 fixation. Science 2005;305:546–95.

Gruber N, Sarmiento JL. Global patterns of marine nitrogen fixation and denitrification. Glob Biogeochem Cycles 1997;11:235–66. 10.1029/97GB00077 DOI

Capone DG, Burns JA, Montoya JPet al. . Nitrogen fixation by Trichodesmium spp.: an important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Glob Biogeochem Cycles 2005;19:2. 10.1029/2004GB002331 DOI

Capone DG, Zehr JP, Paerl HWet al. . Trichodesmium, a globally significant marine cyanobacterium. Science 1997;276:1221–9. 10.1126/science.276.5316.1221 DOI

Sohm JA, Mahaffey C, Capone DG. Assessment of relative phosphorus limitation of Trichodesmium spp. in the North Pacific, North Atlantic, and the north coast of Australia. Limnol Oceanogr 2008;53:2495–502. 10.4319/lo.2008.53.6.2495 DOI

Walsby AE. The gas vesicles and buoyancy of Trichodesmium. In: Carpenter E.J., Capone D.G., Rueter J.G. (eds.), Marine Pelagic Cyanobacteria: Trichodesmium and Other Diazotrophs. Dordrecht: Springer Netherlands, 1992, 141–61.

Benavides M, Bonnet S, Le Moigne FACet al. . Sinking Trichodesmium fixes nitrogen in the dark ocean. ISME J. 2022;16:2398–405. 10.1038/s41396-022-01289-6 PubMed DOI PMC

Pabortsava K, Lampitt RS, Benson Jet al. . Carbon sequestration in the deep Atlantic enhanced by Saharan dust. Nat Geosci 2017;10:189–94. 10.1038/ngeo2899 DOI

Sheridan CC, Steinberg DK, Kling GW. The microbial and metazoan community associated with colonies of Trichodesmium spp.: a quantitative survey. J Plankton Res 2002;24:913–22. 10.1093/plankt/24.9.913 DOI

Hewson I, Poretsky RS, Dyhrman STet al. . Microbial community gene expression within colonies of the diazotroph, Trichodesmium, from the Southwest Pacific Ocean. ISME J. 2009;3:1286–300. 10.1038/ismej.2009.75 PubMed DOI

Borstad GA. Some Aspects of the Occurrence and Biology of Trichodesmium (Cyanophyta) in the Western Tropical Atlantic near Barbados, West Indies PhD thesis. McGill University, Montreal, Canada, 1978.

Hmelo LR, Van Mooy BAS, Mincer TJ. Characterization of bacterial epibionts on the cyanobacterium Trichodesmium. Aquat Microb Ecol 2012;67:1–14. 10.3354/ame01571 DOI

Basu S, Gledhill M, de Beer Det al. . Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust. Commun Biol 2019;2:284. 10.1038/s42003-019-0534-z PubMed DOI PMC

Basu S, Shaked Y. Mineral iron utilization by natural and cultured Trichodesmium and associated bacteria. Limnol Oceanogr 2018;63:2307–20. 10.1002/lno.10939 DOI

Frischkorn KR, Haley ST, Dyhrman ST. Coordinated gene expression between Trichodesmium and its microbiome over day–night cycles in the North Pacific subtropical gyre. ISME J 2018;12:997–1007. 10.1038/s41396-017-0041-5 PubMed DOI PMC

Frischkorn KR, Rouco M, Van Mooy BASet al. . The Trichodesmium microbiome can modulate host N2 fixation. Limnol Oceanogr Lett 2018;3:401–8. 10.1002/lol2.10092 DOI

Rouco M, Haley ST, Dyhrman ST. Microbial diversity within the Trichodesmium holobiont. Environ Microbiol 2016;18:5151–60. 10.1111/1462-2920.13513 PubMed DOI

Frischkorn KR, Rouco M, Van Mooy BASet al. . Epibionts dominate metabolic functional potential of Trichodesmium colonies from the oligotrophic ocean. ISME J 2017;11:2090–101. 10.1038/ismej.2017.74 PubMed DOI PMC

Gradoville MR, Crump BC, Letelier RMet al. . Microbiome of Trichodesmium colonies from the North Pacific subtropical gyre. Front Microbiol 2017;8:8. 10.3389/fmicb.2017.01122 PubMed DOI PMC

Koedooder C, Zhang F, Wang Set al. . Taxonomic distribution of metabolic functions in bacteria associated with Trichodesmium consortia. mSystems 2023;8:e00742–23. 10.1128/msystems.00742-23 PubMed DOI PMC

Keeling PJ, Campo JD. Marine Protists are not just big bacteria. Curr Biol 2017;27:R541–9. 10.1016/j.cub.2017.03.075 PubMed DOI

Eichner M, Inomura K, Pierella Karlusich JJet al. . Better together? Lessons on sociality from Trichodesmium. Trends Microbiol 2023;31:1072–84. 10.1016/j.tim.2023.05.001 PubMed DOI

Anderson OR. Fine structure of a marine Ameba associated with a blue-green alga in the Sargasso Sea. J Protozool. 1977;24:370–6. 10.1111/j.1550-7408.1977.tb04753.x DOI

Page F.C. (ed.). Marine Gymnamoebae. Institute of Terrestrial Ecology, Cambridge, 1983.

Adl SM, Bass D, Lane CEet al. . Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 2019;66:4–119. 10.1111/jeu.12691 PubMed DOI PMC

Rogerson A, Anderson OR, Vogel C. Are planktonic naked amoebae predominately floc associated or free in the water column? J Plankton Res 2003;25:1359–65. 10.1093/plankt/fbg102 DOI

Udalov I. Taxonomy of amoeboid protists: a brief history of research from C. Gessner to T. Cavalier-smith. Protistology 2022;16:68–86. 10.21685/1680-0826-2022-16-2-2 DOI

Kang S, Tice AK, Spiegel FWet al. . Between a pod and a hard test: the deep evolution of amoebae. Mol Biol Evol 2017;34:2258–70. 10.1093/molbev/msx162 PubMed DOI PMC

Held NA, Sutherland KM, Webb EAet al. . Mechanisms and heterogeneity of in situ mineral processing by the marine nitrogen fixer Trichodesmium revealed by single-colony metaproteomics. ISME commun 2021;1:35. 10.1038/s43705-021-00034-y PubMed DOI PMC

Wang S, Koedooder C, Zhang Fet al. . Colonies of the marine cyanobacterium Trichodesmium optimize dust utilization by selective collection and retention of nutrient-rich particles. iScience 2022;25:103587. 10.1016/j.isci.2021.103587 PubMed DOI PMC

Wang S, Zhang F, Koedooder Cet al. . Costs of dust collection by Trichodesmium: effect on buoyancy and toxic metal release. J Geophys Res Biogeosci 2024;129:e2023JG007954. 10.1029/2023JG007954 DOI

Money NP, Fischer MW. What is the weight of a single amoeba and why does it matter? Am Biol Teach 2021;83:571–4. 10.1525/abt.2021.83.9.571 DOI

Bolyen E, Rideout JR, Dillon MRet al. . Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019;37:852–7. 10.1038/s41587-019-0209-9 PubMed DOI PMC

Callahan BJ, McMurdie PJ, Rosen MJet al. . DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 2016;13:581–3. 10.1038/nmeth.3869 PubMed DOI PMC

Quast C, Pruesse E, Yilmaz Pet al. . The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013;41:D590–6. 10.1093/nar/gks1219 PubMed DOI PMC

Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005;71:8228–35. 10.1128/AEM.71.12.8228-8235.2005 PubMed DOI PMC

Chen Y-B, Zehr JP, Mellon M. Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS 101 in defined media: evidence for a circadian rhythm. J Phycol 1996;32:916–23. 10.1111/j.0022-3646.1996.00916.x DOI

Dobashi T. Role of Marine Nitrogen-Fixing Organisms in the Formation of Atmospheric Reactive Nitrogen Doctoral thesis. Hokkaido university, Sapporo, Japan, 2023.

Medlin L, Elwood HJ, Stickel Set al. . The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 1988;71:491–9. 10.1016/0378-1119(88)90066-2 PubMed DOI

Schuster FL. Fine structure of the schizont stage of the testate marine ameba, Trichosphaerium sp. J Protozool. 1976;23:86–93. 10.1111/j.1550-7408.1976.tb05250.x DOI

Koedooder C, Landou E, Zhang Fet al. . Metagenomes of Red Sea subpopulations challenge the use of marker genes and morphology to assess Trichodesmium diversity. Front Microbiol 2022;13:879970. 10.3389/fmicb.2022.879970 PubMed DOI PMC

Tekle YI, Grant J, Anderson ORet al. . Phylogenetic placement of diverse amoebae inferred from multigene analyses and assessment of clade stability within ‘Amoebozoa’ upon removal of varying rate classes of SSU-rDNA. Mol Phylogenetics Evol 2008;47:339–52. 10.1016/j.ympev.2007.11.015 PubMed DOI

Angell RW. Structure of Trichosphaerium micrum sp. n. J Protozool 1975;22:18–22. 10.1111/j.1550-7408.1975.tb00937.x DOI

Angell RW. Observations on Trichosphaerium platyxyrum sp. n. J Protozool 1976;23:357–64. 10.1111/j.1550-7408.1976.tb03788.x DOI

Moran MA, Kujawinski EB, Stubbins Aet al. . Deciphering Ocean carbon in a changing world. Proc Natl Acad Sci 2016;113:3143–51. 10.1073/pnas.1514645113 PubMed DOI PMC

Rogerson A, Hannah F, Gothe G. The grazing potential of some unusual marine benthic amoebae feeding on bacteria. Eur J Protistol 1996;32:271–9. 10.1016/S0932-4739(96)80026-5 DOI

Tekle YI, Tran H, Wang Fet al. . Omics of an enigmatic marine amoeba uncovers unprecedented gene trafficking from giant viruses and provides insights into its complex life cycle. Microbiol Res 2023;14:656–72. 10.3390/microbiolres14020047 PubMed DOI PMC

Polne-Fuller M, Rogerson A, Amano Het al. . Digestion of seaweeds by the marine amoeba Trichosphaerium. Hydrobiologia 1990;204-205:409–13. 10.1007/BF00040264 DOI

Rogerson A, Williams AG, Wilson PC. Utilization of macroalgal carbohydrates by the marine amoeba Trichosphaerium Sieboldi. J Mar Biol Assoc UK 1998;78:733–44. 10.1017/S002531540004474X DOI

Schaudinn FR. Untersuchungen Über den Generationswechsel von "Trichosphaerium Sieboldi" Schn. vol. Berlin Suppl. Abh. Konigl. Preuss. Akad. Wiss, Berlin, Germany, 1899.

Sheehan R, Banner FT. Trichosphaerium—an extraordinary testate Rhizopod from coastal waters. Estuar Coast Mar Sci 1973;1:245–60. 10.1016/0302-3524(73)90038-8 DOI

Cowie PR, Hannah F. Impact of laboratory-imposed physical disturbance on the abundance of four isolates of marine gymnamoebae. Mar Biol 2007;151:675–86. 10.1007/s00227-006-0507-x DOI

Lima PC, Taylor RS, Cook M. Pseudocyst formation in the marine parasitic amoeba Neoparamoeba perurans: a short-term survival strategy to abrupt salinity variation. J Fish Dis 2016;40:1109–13. 10.1111/jfd.12588 PubMed DOI

Moulton M, Suanda SH, Garwood JCet al. . Exchange of plankton, pollutants, and particles across the nearshore region. Annu Rev Mar Sci 2023;15:167–202. 10.1146/annurev-marine-032122-115057 PubMed DOI

Renate E, Edward JC. Association of the copepod Macrosetella gracilis with the cyanobacterium Trichodesmium spp. in the North Pacific gyre. Mar Ecol Prog Ser 2007;333:205–12.

Anderson R. Amoebozoan lobose amoebae (Tubulinea, Flabellinea, and others). Handbook of the Protists 2017;2:1279–309. 10.1007/978-3-319-28149-0_2 DOI

Villareal TA, Carpenter EJ. Diel buoyancy regulation in the marine diazotrophic cyanobacterium Trichodesmium thiebautii. Limnol Oceanogr 1990;35:1832–7. 10.4319/lo.1990.35.8.1832 DOI

Held NA, Waterbury JB, Webb EAet al. . Dynamic diel proteome and daytime nitrogenase activity supports buoyancy in the cyanobacterium Trichodesmium. Nat Microbiol 2022;7:300–11. 10.1038/s41564-021-01028-1 PubMed DOI PMC

Mulholland MR. The fate of nitrogen fixed by diazotrophs in the ocean. Biogeosciences 2007;4:37–51. 10.5194/bg-4-37-2007 DOI

Walsh JJ, Steidinger KA. Saharan dust and Florida red tides: the cyanophyte connection. Journal of Geophysical Research: Oceans 2001;106:11597–612. 10.1029/1999JC000123 DOI

Dupouy C, Benielli-Gary D, Neveux Jet al. . An algorithm for detecting Trichodesmium surface blooms in the south western tropical Pacific. Biogeosciences 2011;8:3631–47. 10.5194/bg-8-3631-2011 DOI

Carpenter EJ. Nitrogen fixation by marine Oscillatoria (Trichodesmium) in the world's oceans. In: Carpenter E.J., Capone D.G. (eds.), Nitrogen in the Marine Environment. Academic Press, New York, 1983, 65–103.

Davies C, Eriksen R, Richardson A. Spatial and seasonal trends in Trichodesmium. In: Richardson A.J., Eriksen R., Moltmann T.et al. (eds.), State and Trends of Australia’s Ocean (STAR), Integrated Marine Observing System (IMOS), Tasmania, 2020, 164.

Dupouy C, Dirgerg G, Tenório Met al. . Surveillance des Trichodesmium autour de la nouvelle-Calédonie, du Vanuatu, de Fidji et de Tonga 1998–2004. Archives Sciences de la Mer 2004;7:51.