Abstract
Symbiotic interactions are widespread in Earth’s ecosystems including the marine environment. “Living together” describes a spectrum of interactions ranging from predation and parasitism to the positive interactions of commensalism and mutualism most commonly associated with the term symbiosis. Many well-known symbioses in the marine environment involve associations between microbes and multicellular organisms such as corals but there are diverse microbe-microbe symbiotic interactions that have been described for decades if not centuries from microscopic observations. Microbe-microbe symbioses have been challenging to study in part because of their small size, our inability to establish and culture them in the laboratory, and the ineffectiveness or inappropriateness of the methods that have been used to study macroscopic species. However, technical advances in nucleic acid sequencing, bioinformatics, isotopic approaches, and imaging have begun to provide new insights into these diverse and abundant interactions. The application of culture-independent approaches has revealed that microbial interactions in the marine microbiome range from metabolite exchanges between free-living planktonic cells to epibiotic and intracellular endosymbiotic interactions that bridge the symbiosis – organelle transition. Here we provide a brief overview of symbiosis and then focus on two specific vignettes in the oceanic plankton—N2-fixing and planktonic rhizarian symbioses—that illustrate how cutting-edge approaches and methodologies are providing new insights into the establishment and functioning of these associations.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alacid E, Reñé A, Garcés E (2015) New insights into the parasitoid Parvilucifera sinerae life cycle: the development and kinetics of infection of a bloom-forming dinoflagellate host. Protist 166:677–699
Alegado RA, Brown LW, Cao S, Dermenjian RK, Zuzow R, Fairclough SR, Clardy J, King N (2012) A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals. eLife 1:e00013
Altenburger A, Cai H, Li Q, Drumm K, Kim M, Zhu Y, Garcia-Cuetos L, Zhan X, Hansen PJ, John U, Li S, Lundholm N (2021) Limits to the cellular control of sequestered cryptophyte prey in the marine ciliate Mesodinium rubrum. ISME J 15:1056–1072
Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT, Heal KR, Morales RL, Berthiaume CT, Parker MS, Djunaedi B, Ingalls AE, Parsek MR, Moran MA, Armbrust EV (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101
Anderson OR (1976) Fine structure of a Collodarian Radiolarian (Sphaerozoum punctatum Müller 1858) and cytoplasmic changes during reproduction. Mar Micropaleontol 1:287–297
Anderson OR (1977) The fine structure of a marine ameba associated with a blue-green alga in the Sargasso Sea. J Protozool 24:370–376
Anderson OR (1978) Fine structure of a symbiont-bearing colonial radiolarian, Collosphaera globularis, and 14C isotopic evidence for assimilation of organic substances from its zooxanthellae. J Ultrastruct Res 62:181–189
Anderson OR (1983a) Radiolaria. Springer, New York, p 355
Anderson OR (1983b) The radiolarian symbiosis. In: Goff LJ (ed) Algal symbiosis. Cambridge University Press, Cambridge, pp 69–89
Anderson OR (1993) The trophic role of planktonic foraminifera and radiolaria. Mar Microb Food Webs 7:31–51
Anderson OR (2014) Living together in the plankton: a survey of marine protist symbioses. Acta Protozool 53:29–38
Anderson OR, Swanberg NR, Bennett P (1983a) Assimilation of symbiont-derived photosynthesis in some solitary and colonial radiolaria. Mar Biol 77:265–269
Anderson OR, Swanberg NR, Bennett P (1983b) Fine structure of yellow-brown symbionts (Prymnesiida) in solitary radiolaria and their comparison with similar acantharian symbionts. J Protozool 30:718–722
Anderson OR, Bennett P, Angel D, Bryan M (1989) Experimental and observational studies of radiolarian physiological ecology: 2. Trophic activity and symbiont primary productivity of Spongaster tetras tetras with comparative data on predatory activity of some Nassellarida. Mar Micropaleontol 14:267–273
Apprill A (2020) The role of symbioses in the adaptation and stress responses of marine organisms. Annu Rev Mar Sci 12:291–314
Archibald JM, Simpson AGB, Slamovits CH (2017) Handbook of the protists. Springer, Cham, p 1657
Balzano S, Corre E, Decelle J, Sierra R, Wincker P, Da Silva C, Poulain J, Pawlowski J, Not F (2015) Transcriptome analyses to investigate symbiotic relationships between marine protists. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00098
Bauer-Nebelsick M, Bardele CF, Ott JA (1996) Redescription of Zoothamnium niveum (Hemprich & Ehrenberg, 1831), Eherenberg 1938 (Oligohymenophora, Peritrichida), a ciliate with ectosymbiotic, chemoautotrophic bacteria. Eur J Protistol 32:18–30
Bé AWH (1982) Biology of planktonic foraminifera. In: Broadhead TW (ed) Foraminifera: notes for a short course. University of Tennessee, Knoxville, pp 51–92
Bé AWH, Anderson OR (1976) Gametogenesis in planktonic foraminifera. Science 192:890–892
Bé AWH, Caron DA, Anderson OR (1981) Effects of feeding frequency on life processes of the planktonic foraminifer Globigerinoides sacculifer in laboratory culture. J Mar Biol Assoc UK 61:257–277
Bé AWH, Spero HJ, Anderson OR (1982) Effects of symbiont elimination and reinfection on the life processes of the planktonic foraminifer Globigerinoides sacculifer. Mar Biol 70:73–86
Bé AWH, Anderson OR, Faber WW Jr, Caron DA (1983) Sequence of morphological and cytoplasmic changes during gametogenesis in the planktonic foraminifer Globigerinoides sacculifer (Brady). Micropaleontology 29:310–325
Bell W, Mitchell R (1972) Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol Bull 143:265–277
Benavides M, Bednarz VN, Ferrier-Pagès C (2017) Diazotrophs: overlooked key players within the coral symbiosis and tropical reef ecosystems? Front Mar Sci. https://doi.org/10.3389/fmars.2017.00010
Berman-Frank I, Lundgren P, Falkowski P (2003) Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol 154:157–164
Berney C, Romac S, Mahe F, Santini S, Siano R, Bass D (2013) Vampires in the oceans: predatory cercozoan amoebae in marine habitats. ISME J 7:2387–2399
Bjorbækmo MFM, Evenstad A, Røsæg LL, Krabberød AK, Logares R (2020) The planktonic protist interactome: where do we stand after a century of research? ISME J 14:544–559
Bombar D, Turk-Kubo KA, Robidart J, Carter BJ, Zehr JP (2013) Non-cyanobacterial nifH phylotypes in the North Pacific Subtropical Gyre detected by flow-cytometry cell sorting. Environ Microbiol Rep 5:705–715. https://doi.org/10.1111/1758-2229.12070
Bothe H, Tripp H, Zehr J (2010) Unicellular cyanobacteria with a new mode of life: the lack of photosynthetic oxygen evolution allows nitrogen fixation to proceed. Arch Microbiol 192:783–790
Böttjer D, Dore JE, Karl DM, Letelier RM, Mahaffey C, Wilson ST, Zehr J, Church MJ (2017) Temporal variability of nitrogen fixation and particulate nitrogen export at Station ALOHA. Limnol Oceanogr 62:200–216
Braga RM (2016) Microbial interactions: ecology in a molecular perspective. Brazil J Microbiol 47S:86–98
Bratbak G, Wilson W, Heldal M (1996) Viral control of Emiliania huxleyi blooms? J Mar Syst 9:75–81
Bråte J, Krabberød AK, Dolven JK, Ose RF, Kristensen T, Bjørklund KR, Shalchian-Tabrizi K (2012) Radiolaria associated with large diversity of marine alveolates. Protist 163:767–777
Breitbart M (2012) Marine viruses: truth or dare. Ann Rev Mar Sci 4:425–448
Buchan A, LeCleir GR, Gulvik CA, Gonzalez JM (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686–698
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 10:693–706
Cachon J, Cachon M (1987) Parasitic dinoflagellates. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell, Oxford, pp 571–610
Cantley AM, Woznica A, Beemelmanns C, King N, Clardy J (2016) Isolation and synthesis of a bacterially produced inhibitor of rosette development in choanoflagellates. J Am Chem Soc 138:4326–4329
Capone DG (1983) N2 fixation in seagrass communities. Mar Technol Soc J 17:32–37
Caputo A, Nylander JA, Foster RA (2019) The genetic diversity and evolution of diatom-diazotroph associations highlights traits favoring symbiont integration. FEMS Microbiol Lett 366:fny297
Cardini U, van Hoytema N, Bednarz VN, Al-Rshaidat MMD, Wild C (2018) N2 fixation and primary productivity in a red sea Halophila stipulacea meadow exposed to seasonality. Limnol Oceanogr 63:786–798
Cardini U, Bartoli M, Lücker S, Mooshammer M, Polzin J, Lee RW, Micić V, Hofmann T, Weber M, Petersen JM (2019) Chemosymbiotic bivalves contribute to the nitrogen budget of seagrass ecosystems. ISME J 13:3131–3134. https://doi.org/10.1038/s41396-019-0486-9
Caron DA, Be AWH, Anderson OR (1982) Effects of variations in light intensity on life processes of the planktonic foraminifer Globigerinoides sacculifer in laboratory culture. J Mar Biol Assoc UK 62:435–451
Caron DA, Faber WW Jr, Bé AWH (1987) Growth of the spinose planktonic foraminifer Orbulina universa in laboratory culture and the effect of temperature on life processes. J Mar Biol Assoc UK 67:343–358
Caron DA, Michaels AF, Swanberg NR, Howse FA (1995) Primary productivity by symbiont-bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda. J Plank Res 17:103–129
Caron DA, Alexander H, Allen AE, Archibald JM, Armbrust EV, Bachy C, Bharti A, Bell CJ, Dyhrman ST, Guida SM, Heidelberg KB, Kaye JZ, Metzner J, Smith SR, Worden AZ (2016) Probing the evolution, ecology and physiology of marine protists using transcriptomics. Nat Rev Microbiol 15:6–20
Carpenter EJ, Culliney JL (1975) Nitrogen fixation in marine shipworms. Science 187:551–552
Carpenter EJ, Janson S (2000) Intracellular cyanobacterial symbionts in the marine diatom Climacodium frauenfeldianum (Bacillariophyceae). J Phycol 36:540–544
Carpenter EJ, Montoya JP, Burns J, Mulholland MR, Subramaniam A, Capone DG (1999) Extensive bloom of a N2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean. Mar Ecol Prog Ser 185:273–283
Chambouvet A, Morin P, Marie D, Guillou L (2008) Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science 322:1254–1257
Childress JJ, Fisher CR (1992) The biology of hydrothermal vent animals—physiology, biochemistry, and autotrophic symbioses. Oceanogr Mar Biol 30:337–441
Coats DW (1999) Parasitic life styles of marine dinoflagellates. J Eukaryot Microbiol 46:402–409
Coats DW, Heisler JJ (1989) Spatial and temporal occurrence of the parasitic dinoflagellate Duboscquella cachoni and its tintinnine host Eutintinnus pectinis in Chesapeake Bay. Mar Biol 101:401–409
Coats DW, Park MG (2002) Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): parasite survival, infectivity, generation time, and host specificity. J Phycol 38:520–528
Cole JJ (1982) Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Syst 13:291–314
Cordero OX, Datta MS (2016) Microbial interactions and community assembly at microscales. Curr Opin Microbiol 31:227–234
Cornejo-Castillo FM, Cabello AM, Salazar G, Sanchez-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
Cornejo-Castillo FM, Munoz-Marin MDC, Turk-Kubo KA, Royo-Llonch M, Farnelid H, Acinas SG, Zehr JP (2019) UCYN-A3, a newly characterized open ocean sublineage of the symbiotic N2-fixing cyanobacterium Candidatus Atelocyanobacterium thalassa. Environ Microbiol 21:111–124
Cruz-López R, Maske H, Yarimizu K, Holland NA (2018) The B-Vitamin mutualism between the dinoflagellate Lingulodinium polyedrum and the bacterium Dinoroseobacter shibae. Front Mar Sci. https://doi.org/10.3389/fmars.2018.00274
Davies-Barnard T, Friedlingstein P (2020) The global distribution of biological nitrogen fixation in terrestrial natural ecosystems. Global Biogeochem Cycles 34:e2019GB006387
Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261
DeBary A (1879) Die Erscheinung der Symbiose. Vortrag auf der Versammlung der Naturforschung und Ärtze zu Kassel. Trübner KJ (ed) Verlag von Karl J Trübner, Strassburg, pp 1–30
Decelle J, Probert I, Bittner L, Desdevises Y, Colin S, de Vargas C, Galí M, Simó R, Not F (2012) An original mode of symbiosis in open ocean plankton. Proc Natl Acad Sci USA 109:18000–18005
Decelle J, Colin S, Forster RA (2015) Photosymbiosis in marine planktonic protists. In: Ohtsuka S, Suzaki T, Horiguchi T, Suzuki N, Not F (eds) Marine protists: diversity and dynamics. Springer, New York, pp 465–500
Decelle J, Stryhanyuk H, Gallet B, Veronesi G, Schmidt M, Balzano S, Marro S, Uwizeye C, Jouneau P-H, Lupette J, Jouhet J, Maréchal E, Schwab Y, Schieber NL, Tucoulou R, Richnow H, Finazzi G, Musat N (2019) Algal remodeling in a ubiquitous planktonic photosymbiosis. Curr Biol 29:968–978.e964
Decelle J, Veronesi G, Gallet B, Stryhanyuk H, Benettoni P, Schmidt M, Tucoulou R, Passarelli M, Bohic S, Clode P, Musat N (2020) Subcellular chemical imaging: new avenues in cell biology. Trends Cell Biol 30:173–188
Decelle J, Veronesi G, LeKieffre C, Gallet B, Chevalier F, Stryhanyuk H, Marro S, Ravanel S, Tucoulou R, Schieber N, Finazzi G, Schwab Y, Musat N (2021) Subcellular architecture and metabolic connection in the planktonic photosymbiosis between Collodaria (radiolarians) and their microalgae. bioRxiv. https://doi.org/10.1101/2021.03.13.435225:2021.2003.2013.435225
Distel DL, DeLong EF, Waterbury JB (1991) Phylogenetic characterization and in situ localization of the bacterial symbiont of shipworms (Teredinidae: Bivalvia) by usiing 16S rRNA sequence analysis and oligodeoxynucleotide probe hybridization. Appl Environ Microbiol 57:2376–2382
Dolan JR (1992) Mixotrophy in ciliates: a review of Chlorella symbiosis and chloroplast retention. Mar Microb Food Webs 6:115–132
Dolven JK, Lindqvist C, Albert VA, Bjørklund KR, Yuasa T, Takahashi O, Mayama S (2007) Molecular diversity of alveolates associated with neritic North Atlantic radiolarians. Protist 158:65–76
Douglas AE, Raven JA (2003) Genomes at the interface between bacteria and organelles. Philos Trans R Soc Lond B Biol Sci 358:5–17. Discussion 517–518
Durham BP, Sharma S, Luo H, Smith CB, Amin SA, Bender SJ, Dearth SP, Van Mooy BA, Campagna SR, Kujawinski EB, Armbrust EV, Moran MA (2015) Cryptic carbon and sulfur cycling between surface ocean plankton. Proc Natl Acad Sci U S A 112:453–457
Egan S, Fukatsu T, Francino MP (2020) Opportunities and challenges to microbial symbiosis research in the microbiome era. Front Microbiol 11:1150
Elmerich C (2007) Historical perspective: from bacterization to endophytes. In: Elmerich C, Newton WE (eds) Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Springer, Dordrecht, pp 1–20
Faber WW Jr, Anderson OR, Lindsey JL, Caron DA (1988) Algal-foraminiferal symbiosis in the planktonic foraminifer Globigerinella aequilateralis: I. Occurrence and stability of two mutually exclusive chrysophyte endosymbionts and their ultrastructure. J Foram Res 18:334–343
Faber WW Jr, Anderson OR, Caron DA (1989) Algal-foraminiferal symbiosis in the planktonic foraminifer Globigerinella aequilateralis: II. Effects of two symbiont species on foraminiferal growth and longevity. J Foram Res 19:185–193
Farnelid H, Tarangkoon W, Hansen G, Hansen PJ, Riemann L (2010) Putative N2-fixing heterotrophic bacteria associated with dinoflagellate–cyanobacteria consortia in the low-nitrogen Indian Ocean. Aquat Microb Ecol 61:105–117
Farnelid H, Turk-Kubo K, Munoz-Marin MD, Zehr JP (2016) New insights into the ecology of the globally significant uncultured nitrogen-fixing symbiont UCYN-A. Aquat Microb Ecol 77:125–138
Farnelid H, Turk-Kubo K, Zehr JP (2020) Cell sorting reveals few novel prokaryote and photosynthetic picoeukaryote associations in the oligotrophic ocean. Environ Microbiol 23:1469–1480. https://doi.org/10.1111/1462-2920.15351
Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56:340–373
Fiore CL, Jarett JK, Olson ND, Lesser MP (2010) Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol 18:455–463
Fisher K, Newton WE (2002) Chapter 1—Nitrogen fixation—a general overview. In: Leigh GJ (ed) Nitrogen fixation at the millennium. Elsevier, Amsterdam, pp 1–34
Floener L, Bothe H (1980) Nitrogen fixation in Rhopalodia gibba, a diatom containing blue-greenish inclusions symbiotically. In: Schwemmler W, Schenk HEA (eds) Endocytobiology, endosymbiosis and cell biology. Walter de Gruyter, New York, pp 541–552
Flynn KJ, Mitra A, Anestis K, Anschütz AA, Calbet A, Ferreira GD, Gypens N, Hansen PJ, John U, Martin JL, Mansour JS, Maselli M, Medić N, Norlin A, Not F, Pitta P, Romano F, Saiz E, Schneider LK, Stolte W, Traboni C (2019) Mixotrophic protists and a new paradigm for marine ecology: where does plankton research go now? J Plank Res 41:375–391
Foster RA, Zehr JP (2006) Characterization of diatom-cyanobacteria symbioses on the basis of nifH, hetR, and 16S rRNA sequences. Environ Microbiol 8:1913–1925
Foster RA, Zehr JP (2019) Diversity, genomics, and distribution of phytoplankton-cyanobacterium single-cell symbiotic associations. Annu Rev Microbiol 73:435–456
Foster RA, Carpenter EJ, Bergman B (2006a) Unicellular cyanobionts in open ocean dinoflagellates, radiolarians, and tintinnids: ultrastructural characterization and immuno-localization of phycoerythrin and nitrogenase. J Phycol 42:453–463
Foster RA, Collier JL, Carpenter EJ (2006b) Reverse transcription PCR amplification of cyanobacterial symbiont 16S rRNA sequences from single non-photosynthetic eukaryotic marine planktonic host cells. J Phycol 42:243–250
Foster RA, Goebel NL, Zehr JP (2010) Isolation of Calothrix rhizosoleniae (Cyanobacteria) strain SC01from Chaetoceros (Bacillariophyta) spp. diatoms of the subtropical north Pacific Ocean. J Phycol 46:1028–1037
Foster RA, Kuypers MMM, Vagner T, Paerl RW, Musat N, Zehr JP (2011) Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. ISME J 5:1484–1493
Frank AB (1877) Über die biologischen Verhältnisse des Thallus einiger Krustenflechten. Beitr Biol Pflanz 2:123–200
Frischkorn KR, Rouco M, Van Mooy BAS, Dyhrman ST (2017) Epibionts dominate metabolic functional potential of Trichodesmium colonies from the oligotrophic ocean. ISME J 11:2090–2101
Fuhrman JA, Suttle CA (1993) Viruses in marine planktonic systems. Oceanography 6:51–63
Garvetto A, Nézan E, Badis Y, Bilien G, Arce P, Bresnan E, Gachon CMM, Siano R (2018) Novel widespread marine oomycetes parasitising diatoms, including the toxic genus Pseudo-nitzschia: genetic, morphological, and ecological characterisation. Front Microbiol. https://doi.org/10.3389/fmicb.2018.02918
Gast RJ (2006) Molecular phylogeny of a potentially parasitic dinoflagellate isolated from the solitary radiolarian, Thalassicolla nucleata. J Euk Microbiol 53:43–45
Gast RJ, Caron DA (1996) Molecular phylogeny of symbiotic dinoflagellates from Foraminifera and Radiolaria. Mol Biol Evol 13:1192–1197
Gast RJ, Caron DA (2001) Photosymbiotic associations in planktonic foraminifera and radiolaria. Hydrobiologia 461:1–7
Gast RJ, McDonnell TA, Caron DA (2000) srDNA-based taxonomic affinities of algal symbionts from a planktonic foraminifer and a solitary radiolarian. J Phycol 36:172–177
Gast RJ, Moran DM, Dennett MR, Caron DA (2007) Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition? Environ Microbiol 9:39–45
Gomaa F, Kosakyan A, Heger T, Corsaro D, Mitchell E, Lara E (2014) One alga to rule them all: unrelated mixotrophic testate amoebae (Amoebozoa, Rhizaria and stramenopiles) share the same symbiont (Trebouxiophyceae). Protist 165(2):161–176
Gradoville MR, Crump BC, Letelier RM, Church MJ, White AE (2017) Microbiome of Trichodesmium Colonies from the North Pacific Subtropical Gyre. Front Microbiol 8:1122
Greco M, Morard R, Kucera M (2021) Single-cell metabarcoding reveals biotic interactions of the Arctic calcifier Neogloboquadrina pachyderma with the eukaryotic pelagic community. J Plank Res 43:113–125
Groisillier A, Massana R, Valentin K, Vaulot D, Guillou L (2006) Genetic diversity and habitats of two enigmatic marine alveolate lineages. Aquat Microb Ecol 42:277–291
Guerrero R, Pedros-Alio C, Esteve I, Mas J, Chase D, Margulis L (1986) Predatory prokaryotes: predation and primary consumption evolved in bacteria. Proc Natl Acad Sci U S A 83:2138–2142
Guillou L, Viprey M, Chambouvet A, Welsh RM, Kirkham AR, Massana R, Scanlan DJ, Worden AZ (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol 10:3349–3365
Haeckel E (1862) Die Radiolarien (Rhizopoda Radiaria). Eine Monographie, Reimer, Berlin
Haeckel E (1887) Report on Radiolaria collected by H.M.S. Challenger during the 1873-1876. In: Thompson CW, Murray J (eds) The voyage of the HMS Challenger. Her Majesty’s Stationary Office, London, pp 1–1760
Hagino K, Onuma R, Kawachi M, Horiguchi T (2013) Discovery of an endosymbiotic nitrogen-fixing cyanobacterium UCYN-A in Braarudosphaera bigelowii (Prymnesiophyceae). PLoS One 8:e81749
Hanic LA, Sekimoto S, Bates SS (2009) Oomycete and chytrid infections of the marine diatom Pseudo-nitzschia pungens (Bacillariophyceae) from Prince Edward Island, Canada. Botany 87:1096–1105
Haq B, Boersma A (eds) (1998) Introduction to marine micropaleontology. Elsevier, Amsterdam, 376p
Harding K, Turk-Kubo KA, Sipler RE, Mills MM, Bronk DA, Zehr JP (2018) Symbiotic unicellular cyanobacteria fix nitrogen in the Arctic Ocean. Proc Natl Acad Sci U S A 115:13371–13375
Harke MJ, Frischkorn KR, Haley ST, Aylward FO, Zehr JP, Dyhrman ST (2019) Periodic and coordinated gene expression between a diazotroph and its diatom host. ISME J 13:118–131
Head WD, Carpenter EJ (1975) Nitrogen fixation associated with the marine macroalga Codium fragile. Limnol Oceanogr 20:815–823
Heide T, Govers L, de Fouw J, Olff H, Van der Geest M, Katwijk M, Piersma T, van de Koppel J, Silliman B, Smolders A, Van Gils J (2012) A three-stage symbiosis forms the foundation of seagrass ecosystems. Science 336:1432–1434
Hemleben C, Spindler M, Anderson OR (1988) Modern planktonic foraminifera. Springer, New York, p 363
Heninbokel JF (1986) Occurrence of Richelia intracellularis (Cyanophyta) within diatoms Hemiaulus hauckii and H. membranaceus off Hawaii. J Phycol 22:399–403
Hertwig R (1879) Der Organismus der Radiolarien. Jena Denksch 2:129–277
Hess S (2017) Hunting for agile prey: trophic specialisation in leptophryid amoebae (Vampyrellida, Rhizaria) revealed by two novel predators of planktonic algae. FEMS Microbiol Ecol 93. https://doi.org/10.1093/femsec/fix104
Hewson I, Poretsky RS, Dyhrman ST, Zielinkski B, White AE, Tripp HJ, Montoya JP, Zehr JP (2009) Microbial community gene expression within colonies of the diazotroph, Trichodesmium, from the Southwest Pacific Ocean. ISME J 3:1286–1300
Hilton JA, Foster RA, Tripp HJ, Carter BJ, Zehr JP, Villareal TA (2013) Genomic deletions disrupt nitrogen metabolism pathways of a cyanobacterial diatom symbiont. Nat Commun 4:1767
Hilton JA, Satinsky BM, Doherty M, Zielinski B, Zehr JP (2015) Metatranscriptomics of N2-fixing cyanobacteria in the Amazon River plume. ISME J 9:1557–1569
Hinde R, Smith DC (1974) “Chloroplast symbiosis” and the extent to which it occurs in Saccoglossa (Gastropoda: Mollusca). Biol J Linnean Soc 6:349–356
Janson S, Wouters J, Bergman B, Carpenter EJ (1999) Host specificity in the Richelia-diatom symbiosis revealed by hetR gene sequence analysis. Environ Microbiol 1:431–438
Johansson ON, Pinder MIM, Ohlsson F, Egardt J, Töpel M, Clarke AK (2019) Friends with benefits: exploring the phycosphere of the marine diatom Skeletonema marinoi. Front Microbiol. https://doi.org/10.3389/fmicb.2019.01828
Johnson MD, Oldach D, Delwiche CF, Stoecker DK (2007) Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445:426–428
Johnson MD, Lasek-Nesselquist E, Moeller HV, Altenburger A, Lundholm N, Kim M, Drumm K, Moestrup Ø, Hansen PJ (2017) Mesodinium rubrum: the symbiosis that wasn’t. Proc Natl Acad Sci USA 114:E1040–E1042
Jørgensen BB, Erez J, Revsbech NP, Cohen Y (1985) Symbiotic photosynthesis in a planktonic foraminiferan, Globigerinoides sacculifer (Brady), studied with microelectrodes. Limnol Oceanogr 30:1253–1267
Kagami M, de Bruin A, Ibelings BW, Van Donk E (2007) Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578:113–129
Karl D, Letelier R, Tupas L, Dore J, Christian J, Hebel D (1997) The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388:533–538
Karlusich JJP, Pelletier E, Carsique M, Dvorak E, Colin S, Picheral M, Pepperkok R, Karsenti E, Vargas Cd, Lombard F, Wincker P, Bowler C, Foster RA (2020) Global distribution patterns of marine nitrogen-fixers by imaging and molecular methods. bioRxiv. https://doi.org/10.1101/2020.10.17.343731:2020.2010.2017.343731
Keeling PJ, McCutcheon JP, Doolittle WF (2015) Symbiosis becoming permanent: survival of the luckiest. Proc Natl Acad Sci USA 112:10101–10103
Kiers ET, West SA (2015) Evolutionary biology. Evolving new organisms via symbiosis. Science 348:392–394
Kim S, Jeon CB, Park MG (2017) Morphological observations and phylogenetic position of the parasitoid nanoflagellate Pseudopirsonia sp. (Cercozoa) infecting the marine diatom Coscinodiscus wailesii (Bacillariophyta). Algae 32:181–187
Kimoto K (2015) Planktonic foraminifera. In: Ohtsuka S, Suzaki T, Horiguchi T, Suzuki N, Not F (eds) Marine protists: diversity and dynamics. Springer, New York, pp 129–178
King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemon D, Wanqing L, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Bork P, Lim WA, Manning F, Miller WT, McGinnis W, Shapiro H, Tijian R, Grigoriev IV, Rokhsar D (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783–788
Krupke A, Musat N, LaRoche J, Mohr W, Fuchs BM, Amann RI, Kuypers MMM, Foster RA (2013) In situ identification and N2 and C fixation rates of uncultivated cyanobacteria populations. Syst Appl Microbiol 36:259–271
Krupke A, Lavik G, Halm H, Fuchs BM, Amann RI, Kuypers MMM (2014) Distribution of a consortium between unicellular algae and the N2 fixing cyanobacterium UCYN-A in the North Atlantic Ocean. Environ Microbiol 16:3153–3167
Kühn SF (1998) Infection of Coscinodiscus spp. by the parasitoid nanoflagellate Pirsonia diadema: II. Selective infection behaviour for host species and individual host cells. J Plank Res 20:443–454
Kühn S, Medlin L, Eller G (2004) Phylogenetic position of the parasitoid nanoflagellate Pirsonia inferred from nuclear-encoded small subunit ribosomal DNA and a description of Pseudopirsonia n. gen. and Pseudopirsonia mucosa (Drebes) comb. nov. Protist 155:143–156
Lasek-Nesselquist E, Wisecaver JH, Hackett JD, Johnson MD (2015) Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum. BMC Genomics 16:805
Lee MD, Webb EA, Walworth NG, Fu F-X, Held NA, Saito MA, Hutchins DA (2018) Transcriptional activities of the microbial consortium living with the marine nitrogen-fixing cyanobacterium Trichodesmium reveal potential roles in community-level nitrogen cycling. Appl Environ Microbiol 84:e02026–e02017
LeKieffre C, Spero HJ, Russell AD, Fehrenbacher JS, Geslin E, Meibom A (2018) Assimilation, translocation, and utilization of carbon between photosynthetic symbiotic dinoflagellates and their planktic foraminifera host. Mar Biol 165:104
Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, Chaffron S, Ignacio-Espinosa JC, Roux S, Vincent F, Bittner L, Darzi Y, Wang J, Audic S, Berline L, Bontempi G, Cabello AM, Coppola L, Cornejo-Castillo FM, d’Ovidio F, De Meester L, Ferrera I, Garet-Delmas M-J, Guidi L, Lara E, Pesant S, Royo-Llonch M, Salazar G, Sánchez P, Sebastian M, Souffreau C, Dimier C, Picheral M, Searson S, Kandels-Lewis S, Tara Oceans Coordinators, Gorsky G, Not F, Ogata H, Speich S, Stemmann L, Weissenbach J, Wincker P, Acinas SG, Sunagawa S, Bork P, Sullivan MB, Karsenti E, Bowler C, de Vargas C, Raes J (2015) Determinants of community structure in the global plankton interactome. Science 348:1262073-1262071–1262073-1262079
Liu Z, Mesrop LY, Hu SK, Caron DA (2019) Transcriptome of Thalassicolla nucleata holobiont reveals details of a radiolarian symbiotic relationship. Front Mar Sci. https://doi.org/10.3389/fmars.2019.00284
Lucas IAN (1991) Symbionts of the tropical Dinophysiales (Dinophyceae). Ophelia 33:213–224
Mackiewicz P, Bodył A, Gagat P (2012) Protein import into the photosynthetic organelles of Paulinella chromatophora and its implications for primary plastid endosymbiosis. Symbiosis 58:99–107
Martinez-Perez C, Mohr W, Loscher CR, Dekaezemacker J, Littmann S, Yilmaz P, Lehnen N, Fuchs BM, Lavik G, Schmitz RA, LaRoche J, Kuypers MM (2016) The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle. Nat Microbiol 1:16163
Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51:139–144
McFall-Ngai M (2014) Divining the essence of symbiosis: insights from the squid-Vibrio model. PLoS Biol 12:e1001783
Meheust R, Zelzion E, Bhattacharya D, Lopez P, Bapteste E (2016) Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis. Proc Natl Acad Sci U S A 113:3579–3584
Meyer E, Weis VM (2012) Study of cnidarian-algal symbiosis in the “omics” age. Biol Bull 223:44–65
Michaels AF (1991) Acantharian abundance and symbiont productivity at the VERTEX seasonal station. J Plank Res 13:399–418
Mills MM, Turk-Kubo KA, van Dijken GL, Henke BA, Harding K, Wilson ST, Arrigo KR, Zehr JP (2020) Unusual marine cyanobacteria/haptophyte symbiosis relies on N2 fixation even in N-rich environments. ISME J 14:2395–2406
Mitra A, Flynn KJ, Burkholder JM, Berge T, Calbet A, Raven JA, Granéli E, Glibert PM, Hansen PJ, Stoecker DK, Thingstad F, Tillmann U, Våge S, Wilken S, Zubkov MV (2014) The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11:995–1005
Momper LM, Reese BK, Carvalho G, Lee P, Webb EA (2015) A novel cohabitation between two diazotrophic cyanobacteria in the oligotrophic ocean. ISME J 9:882–893
Monteil CL, Vallenet D, Menguy N, Benzerara K, Barbe V, Fouteau S, Cruaud C, Floriani M, Viollier E, Adryanczyk G, Leonhardt N, Faivre D, Pignol D, López-García P, Weld RJ, Lefevre CT (2019) Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist. Nat Microbiol 4:1088–1095
Moon-van der Staay SY, De Wachter R, Vaulot D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409:607–610
Nakayama T, Ikegami Y, Nakayama T, Ishida K-i, Inagaki Y, Inouye I (2011) Spheroid bodies in rhopalodiacean diatoms were derived from a single endosymbiotic cyanobacterium. J Plant Res 124:93–97
Nakayama T, Kamikawa R, Tanifuji G, Kashiyama Y, Ohkouchi N, Archibald JM, Inagaki Y (2014) Complete genome of a nonphotosynthetic cyanobacterium in a diatom reveals recent adaptations to an intracellular lifestyle. Proc Natl Acad Sci USA 111(31):11407–11412
Norris RD (1996) Symbiosis as an evolutionary innovation in the radiation of Paleocene planktic foraminifera. Paleobiology 22:461–480
Not F, Probert I, Ribiero CG, Crenn K, Guillou L, Jeanthon C, Vaulot D (2016) Photosymbiosis in marine pelagic environments. In: Stal LJ, Cretoiu MS (eds) The marine microbiome. Springer, Cham, pp 305–330
Nowack EC, Grossman AR (2012) Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci U S A 109:5340–5345
Nowack EC, Melkonian M (2010) Endosymbiotic associations within protists. Philos Trans R Soc Lond B Biol Sci 365:699–712
Ochman H, Moran NA (2001) Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292:1096–1099
O’Malley MA (2015) Endosymbiosis and its implications for evolutionary theory. Proc Natl Acad Sci U S A 112:10270–10277
Pasternak Z, Pietrokovski S, Rotem O, Gophna U, Lurie-Weinberger MN, Jurkevitch E (2013) By their genes ye shall know them: genomic signatures of predatory bacteria. ISME J 7:756–769
Paul C, Mausz MA, Pohnert G (2013) A co-culturing/metabolomics approach to investigate chemically mediated interactions of planktonic organisms reveals influence of bacteria on diatom metabolism. Metabolomics 9:349–359
Petersen JM, Kemper A, Gruber-Vodicka H, Cardini U, Van Der Geest M, Kleiner M, Bulgheresi S, Mußmann M, Herbold C, Seah BK (2017) Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation. Nat Microbiol 2:16195
Postgate JR (1998) Nitrogen fixation. Cambridge University Press, Cambridge, UK, p 112
Prechtl J, Kneip C, Lockhart P, Wenderoth K, Maier UG (2004) Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. Mol Biol Evol 21:1477–1481
Probert I, Siano R, Poirier C, Decelle J, Biard T, Tuji A, Suzuki N, Not F (2014) Brandtodinium gen. nov. and B. nutricula comb. Nov. (Dinophyceae), a dinoflagellate commonly found in symbiosis with polycystine radiolarians. J Phycol 50:388–399
Pyle AE, Johnson AM, Villareal TA (2020) Isolation, growth, and nitrogen fixation rates of the Hemiaulus-Richelia (diatom-cyanobacterium) symbiosis in culture. PeerJ 8:e10115
Rai AN, Bergman B, Rasmussen U (2003) Cyanobacteria in symbiosis. Kluwer, New York, p 355
Ramanan R, Kim BH, Cho DH, Oh HM, Kim HS (2016) Algae-bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 34:14–29
Rosset SL, Oakley CA, Ferrier-Pagès C, Suggett DJ, Weis VM, Davy SK (2020) The molecular language of the cnidarian–dinoflagellate symbiosis. Trends Microbiol 29:320–333. https://doi.org/10.1016/j.tim.2020.08.005
Sapp J (2004) The dynamics of symbiosis: an historical overview. Can J Bot 82:1046–1056
Sapp M, Schwaderer AS, Wiltshire KH, Hoppe HG, Gerdts G, Wichels A (2007) Species-specific bacterial communities in the phycosphere of microalgae? Microb Ecol 53:683–699
Schäfer H, Abbas B, Witte H, Muyzer G (2002) Genetic diversity of ‘satellite’ bacteria present in cultures of marine diatoms. FEMS Microbiol Ecol 42:25–35
Scholz B, Guillou L, Marano AV, Neuhauser S, Sullivan BK, Karsten U, Küpper FC, Gleason FH (2016) Zoosporic parasites infecting marine diatoms—a black box that needs to be opened. Fungal Ecol 19:59–76
Schvarcz CR, Wilson ST, Caffin M, Stancheva R, Li Q, Turk-Kubo KA, White AE, Karl DM, Zehr JP, Steward GF (in press) Overlooked and widespread pennate diatom-diazotroph symbioses in the sea. Nat Commun
Seymour JR, Amin SA, Raina JB, Stocker R (2017) Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat Microbiol 2:17065
Shaked Y, de Vargas C (2006) Pelagic photosymbiosis: rDNA assessment of diversity and evolution of dinoflagellate symbionts and planktonic foraminiferal hosts. Mar Ecol Prog Ser 325:59–71
Sheridan CC, Steinberg DK, Kling GW (2002) The microbial and metazoan community associated with colonies of Trichodesmium spp.: a quantitative survey. J Plank Res 24:913–922
Siano R, Montresor M, Probert I, Not F, de Vargas C (2010) Pelagodinium gen. nov. and P. bèii comb. nov., a dinoflagellate symbiont of planktonic foraminifera. Protist 161:385–399
Siddiqui PJA, Bergman B, Carpenter EJ (1992) Filamentous cyanobacterial associates of the marine planktonic cyanobacterium Trichodesmium. Phycologia 31:326–337
Sierra R, Matz MV, Aglyamova G, Pillet L, Decelle J, Not F, de Vargas C, Pawlowski J (2013) Deep relationships of Rhizaria revealed by phylogenomics: a farewell to Haeckel’s Radiolaria. Mol Phyl Evol 67:53–59
Singer A, Poschmann G, Mühlich C, Valadez-Cano C, Hänsch S, Hüren V, Rensing SA, Stühler K, Nowack ECM (2017) Massive protein import into the early-evolutionary-stage photosynthetic organelle of the amoeba Paulinella chromatophora. Curr Biol 27:2763–2773.e2765
Smriga S, Fernandez VI, Mitchell JG, Stocker R (2016) Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria. Proc Natl Acad Sci U S A 113:1576–1581
Sockett RE (2009) Predatory lifestyle of Bdellovibrio bacteriovorus. Annu Rev Microbiol 63:523–539
Spero HJ (1987) Symbiosis in the planktonic foraminfer, Orbulina universa, and the isolation of its symbiotic dinoflagellate, Gymnodinium beii sp. nov. J Phycol 23:307–317
Spero HJ, Parker SL (1985) Photosynthesis in the symbiotic planktonic foraminifer Orbulina universa, and its potential contribution to oceanic primary productivity. J Foram Res 15:273–281
Stickney HL, Hood RR, Stoecker DK (2000) The impact of mixotrophy on planktonic marine ecosystems. Ecol Model 125:203–230
Stocker R (2012) Marine microbes see a sea of gradients. Science 338:628–633
Stoecker DK (1999) Mixotrophy among dinoflagellates. J Eukaryot Microbiol 46:397–401
Stoecker DK, Swanberg N, Tyler S (1989) Oceanic mixotrophic flatworms. Mar Ecol Prog Ser 58:41–51
Stoecker DK, Buck KR, Putt M (1993) Changes in the sea-ice brine community during the spring-summer transition, McMurdo Sound, Antarctica. 2. Phagotrophic protists. Mar Ecol Prog Ser 95:103–113
Stoecker DK, Hansen PJ, Caron DA, Mitra A (2017) Mixotrophy in the marine plankton. Annu Rev Mar Sci 9:331–335
Swanberg NR (1979) The ecology of colonial radiolarians: their colony morphology, trophic interactions and associations, behavior, distribution and the photosynthesis of their symbionts. Ph.D., Woods Hole Oceanographic Institution and Massachusetts Institute of Technology
Swanberg NR (1983) The trophic role of colonial Radiolaria in oligotrophic oceanic environments. Limnol Oceanogr 28:655–666
Swanberg NR, Caron DA (1991) Patterns of sarcodine feeding in epipelagic oceanic plankton. J Plank Res 13:287–312
Swanberg NR, Anderson OR, Lindsey JL, Bennett P (1986) The biology of Physematium muelleri: trophic activity. Deep-Sea Res 33:913–922
Takagi H, Kimoto K, Fujiki T, Kurasawa A, Moriya K, Hirano H (2016) Ontogenetic dynamics of photosymbiosis in cultured planktic foraminifers revealed by fast repetition rate fluorometry. Mar Micropaleontol 122:44–52
Takagi H, Kimoto K, Fujiki T, Moriya K (2018) Effect of nutritional condition on photosymbiotic consortium of cultured Globigerinoides sacculifer (Rhizaria, Foraminifera). Symbiosis 76:25–39
Takagi H, Kimoto K, Fujiki T, Saito H, Schmidt C, Kucera M, Moriya K (2019) Characterizing photosymbiosis in modern planktonic foraminifera. Biogeosciences 16:3377–3396
Takayama T (1972) A note on the distribution of Braarudosphaera bigelowii (Gran and Braarud) Deflandre in the bottom sediments of Sendai Bay, Japan. Trans Proc Palaeont Soc Jpn 87:429–435
Tamm SL (1982) Flagellated ectosymbiotic bacteria propel a eukaryotic cell. J Cell Biol 94:697–709
Taylor FJR (1982) Symbioses in marine microplankton. Ann Inst Océanogr Paris 58(S):61–90
Thompson AW, Zehr JP (2013) Cellular interactions: lessons from the nitrogen-fixing cyanobacteria. J Phycol 49:1024–1035
Thompson AW, Foster RA, Krupke A, Carter BJ, Musat N, Vaulot D, Kuypers MMM, Zehr JP (2012) Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337:1546–1550
Tillmann U, Hesse K-J, Tillmann A (1999) Large-scale parasitic infection of diatoms in the Northfrisian Wadden Sea. J Sea Res 42:255–261
Tomaru Y, Kimura K, Nagasaki K (2015) Marine protist viruses. In: Ohtsuka S, Suzaki T, Horiguchi T, Suzuki N, Not F (eds) Marine protists: diversity and dynamics. Springer, Tokyo, pp 501–517
Trapp EM, Adler S, Zauner S, Maier U-G (2012) Rhopalodia gibba and its endosymbionts as a model for early steps in a cyanobacterial primary endosymbiosis. J Endocyt Cell Res 23:21–24
Tripp HJ, Bench SR, Turk KA, Foster RA, Desany BA, Niazi F, Affourtit JP, Zehr JP (2010) Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature 464:90–94
Ushida K (2018) Symbiotic methanogens and rumen ciliates. In: Hackstein JHP (ed) (Endo)symbiotic methanogenic archaea. Springer, Cham, pp 25–35
Uwizeye C, Mars Brisbin M, Gallet B, Chevalier F, LeKieffre C, Schieber N, Denis F, Wangpraseurt D, Schertel L, Stryhanyuk H, Musat N, Mitarai S, Schwab Y, Finazzi G, Decelle J (2020) Cytoklepty in the plankton: a host strategy to optimize the bioenergetic machinery of endosymbiotic algae. bioRxiv. https://doi.org/10.1101/2020.12.08.416644:2020.2012.2008.416644
Valentine AJ, Benedito VA, Kang Y (2018) Legume nitrogen fixation and soil abiotic stress: from physiology to genomics and beyond. Annu Plant Rev 42:207–248
Villareal T (1989) Division cycles in the nitrogen-fixing Rhizosolenia (Bacillariophyceae)-Richelia (Nostocaceae) symbiosis. Br Phycol J 24:357–365
Villareal TA (1990) Laboratory cultivation and preliminary characterization of the nitrogen - fixing Rhizosolenia - Richelia symbiosis. Mar Ecol 11:117–132
Villareal TA (1991) Nitrogen-fixation by the cyanobacterial symbiont of the diatom genus Hemiaulus. Mar Ecol Prog Ser 76:201–204
Villareal TA (1992) Marine nitrogen-fixing diatom - cyanobacteria symbioses. In: Carpenter EJ, Capone DG, Rueter JG (eds) Marine pelagic cyanobacteria: Trichodesmium and other diazotrophs. Kluwer, Dordrecht, pp 163–175
Villareal TA (1994) Widespread occurrence of the Hemiaulus-cyanobacterial symbiosis in the southwest North Atlantic ocean. Bull Mar Sci 54:1–7
Villareal T, Adornato L, Wilson C, Shoenbachler C (2011) Summer blooms of diatom-diazotroph assemblages (DDAs) and surface chlorophyll in the N. Pacific gyre—a disconnect. J Geophys Res Oceans 116(C3):e6268
Vogels GD, Hoppe WF, Stumm CK (1980) Association of methanogenic bacteria with rumen ciliates. Appl Environ Microbiol 40:608–612
Vorobev A, Dupouy M, Carradec Q, Delmont TO, Annamalé A, Wincker P, Pelletier E (2020) Transcriptome reconstruction and functional analysis of eukaryotic marine plankton communities via high-throughput metagenomics and metatranscriptomics. Genome Res 30:647–659
Wang Z, Wu M (2014) Phylogenomic reconstruction indicates mitochondrial ancestor was an energy parasite. PLoS One 9:e110685
Ward BA, Follows MJ (2016) Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. Proc Natl Acad Sci USA 113:2958–2963
Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181
Wernegreen JJ (2017) In it for the long haul: evolutionary consequences of persistent endosymbiosis. Curr Opin Genet Dev 47:83–90
White AE, Prahl FG, Letelier RM, Popp BN (2007) Summer surface waters in the Gulf of California: prime habitat for biological N2 fixation. Glob Biogeochem Cycle 21:GB2017. https://doi.org/10.1029/2006gb002779
Woznica A, Cantley AM, Beemelmanns C, Freinkman E, Clardy J, King N (2016) Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates. Proc Natl Acad Sci USA 113:7894–7899
Wrede C, Dreier A, Kokoschka S, Hoppert M (2012) Archaea in symbioses. Archaea (Vancouver, BC) 2012:596846
Yarimizu K, Cruz-López R, Carrano CJ (2018) Iron and harmful algae blooms: potential algal-bacterial mutualism between Lingulodinium polyedrum and Marinobacter algicola. Front Mar Sci. https://doi.org/10.3389/fmars.2018.00180
Zehr JP (2015) How single cells work together. Science 349:1163–1164
Zehr JP, Capone DG (2020) Changing perspectives in marine nitrogen fixation. Science 368:eaay9514
Zehr JP, Capone DG (2021) Marine nitrogen fixation. Springer, Cham, p 186
Zehr J, Mellon M, Zani S (1998) New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Appl Environ Microbiol 64:34443450
Zehr JP, Shilova IN, Farnelid HM, Muñoz-Marín MD, Turk-Kubo KA (2016) Unusual marine unicellular symbiosis with the nitrogen-fixing cyanobacterium UCYN-A. Nat Microbiol 2:16214
Zehr JP, Weitz JS, Joint I (2017) How microbes survive in the open ocean. Science 357:646–647
Acknowledgments
This work was partially supported by the Simons Foundation grants (SCOPE 724220 to JPZ, 824082 to JPZ, and P49802 to DAC) and NSF grants (OCE-1559165 to JPZ, and OCE-1737409 to DAC). We thank K. Hagino and C. Schvarcz for providing unpublished images, Andrea Dingeldein for graphic art, and M. R. Gradoville and K. Turk-Kubo for reviewing the manuscript.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Zehr, J.P., Caron, D.A. (2022). Symbiosis in the Ocean Microbiome. In: Stal, L.J., Cretoiu, M.S. (eds) The Marine Microbiome. The Microbiomes of Humans, Animals, Plants, and the Environment, vol 3. Springer, Cham. https://doi.org/10.1007/978-3-030-90383-1_13
Download citation
DOI: https://doi.org/10.1007/978-3-030-90383-1_13
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-90382-4
Online ISBN: 978-3-030-90383-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)