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Abstract

The holobiont concept (i.e., multiple living beings in close symbiosis with one another and functioning as a unit) is revolutionizing our understanding of biology, especially in marine systems. The earliest marine holobiont was likely a syntrophic partnership of at least two prokaryotic members. Since then, symbiosis has enabled marine organisms to conquer all ocean habitats through the formation of holobionts with a wide spectrum of complexities. However, most scientific inquiries have focused on isolated organisms and their adaptations to specific environments. In this review, we attempt to illustrate why a holobiont perspective—specifically, the study of how numerous organisms form a discrete ecological unit through symbiosis—will be a more impactful strategy to advance our understanding of the ecology and evolution of marine life. We argue that this approach is instrumental in addressing the threats to marine biodiversity posed by the current global environmental crisis.

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2024-01-17
2024-04-27
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Literature Cited

  1. Althoff DM, Segraves KA, Johnson MTJ. 2014. Testing for coevolutionary diversification: linking pattern with process. Trends Ecol. Evol. 29:28289
    [Google Scholar]
  2. Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT et al. 2015. Interaction and signaling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:755498101
    [Google Scholar]
  3. Amos B, Aurrecoechea C, Barba M, Barreto A, Basenko EY et al. 2022. VEuPathDB: the eukaryotic pathogen, vector and host bioinformatics resource center. Nucleic Acids Res. 50:D1D898911
    [Google Scholar]
  4. Apprill A. 2020. The role of symbioses in the adaptation and stress responses of marine organisms. Annu. Rev. Mar. Sci. 12:291314
    [Google Scholar]
  5. Archibald J. 2014. One Plus One Equals One: Symbiosis and the Evolution of Complex Life Oxford, UK: Oxford Univ. Press
  6. Arroyo AS, Iannes R, Bapteste E, Ruiz-Trillo I. 2020. Gene similarity networks unveil a potential novel unicellular group closely related to animals from the Tara Oceans expedition. Genome Biol. Evol. 12:9166478
    [Google Scholar]
  7. Asplund ME, Baden SP, Russ S, Ellis RP, Gong N, Hernroth BE. 2014. Ocean acidification and host-pathogen interactions: blue mussels, Mytilus edulis, encountering Vibrio tubiashii. Environ. Microbiol. 16:4102939
    [Google Scholar]
  8. Athanasopoulou K, Boti MA, Adamopoulos PG, Skourou PC, Scorilas A. 2021. Third-generation sequencing: the spearhead towards the radical transformation of modern genomics. Life 12:130
    [Google Scholar]
  9. Avila-Magaña V, Kamel B, DeSalvo M, Gómez-Campo K, Enríquez S et al. 2021. Elucidating gene expression adaptation of phylogenetically divergent coral holobionts under heat stress. Nat. Commun. 12:15731
    [Google Scholar]
  10. Balakirev ES, Krupnova TN, Ayala FJ. 2012. Symbiotic associations in the phenotypically-diverse brown alga Saccharina japonica. PLOS ONE 7:6e39587
    [Google Scholar]
  11. Balakirev ES, Pavlyuchkov VA, Ayala FJ. 2008. DNA variation and symbiotic associations in phenotypically diverse sea urchin Strongylocentrotus intermedius. PNAS 105:421621823
    [Google Scholar]
  12. Barak-Gavish N, Dassa B, Kuhlisch C, Nussbaum I, Brandis A et al. 2023. Bacterial lifestyle switch in response to algal metabolites. eLife 12:e84400
    [Google Scholar]
  13. Barr JJ, Youle M, Rohwer F. 2013. Innate and acquired bacteriophage-mediated immunity. Bacteriophage 3:3e25857
    [Google Scholar]
  14. Beinart RA, Beaudoin DJ, Bernhard JM, Edgcomb VP. 2018. Insights into the metabolic functioning of a multipartner ciliate symbiosis from oxygen-depleted sediments. Mol. Ecol. 27:81794807
    [Google Scholar]
  15. Ben-Dor Cohen E, Ilan M, Yarden O. 2021. The culturable mycobiome of mesophotic Agelas oroides: constituents and changes following sponge transplantation to shallow water. J. Fungi 7:7567
    [Google Scholar]
  16. Bhadury P, Bik H, Lambshead JD, Austen MC, Smerdon GR, Rogers AD. 2011. Molecular diversity of fungal phylotypes co-amplified alongside nematodes from coastal and deep-sea marine environments. PLOS ONE 6:10e26445
    [Google Scholar]
  17. Bhattacharya D, Van Etten J, Benites LF, Stephens TG. 2023. Endosymbiotic ratchet accelerates divergence after organelle origin: the Paulinella model for plastid evolution. BioEssays 45:1e2200165
    [Google Scholar]
  18. Bidle KD, Vardi A. 2011. A chemical arms race at sea mediates algal host-virus interactions. Curr. Opin. Microbiol. 14:444957
    [Google Scholar]
  19. Bojko B, Onat B, Boyaci E, Psillakis E, Dailianis T, Pawliszyn J. 2019. Application of in situ solid-phase microextraction on Mediterranean sponges for untargeted exometabolome screening and environmental monitoring. Front. Mar. Sci. 6:632
    [Google Scholar]
  20. Bordenstein SR, Theis KR. 2015. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLOS Biol. 13:8e1002226Provides in-depth definitions of holobiont and hologenome concepts.
    [Google Scholar]
  21. Breitbart M. 2012. Marine viruses: truth or dare. Annu. Rev. Mar. Sci. 4:42548
    [Google Scholar]
  22. Breusing C, Johnson SB, Tunnicliffe V, Clague DA, Vrijenhoek RC, Beinart RA. 2020. Allopatric and sympatric drivers of speciation in Alviniconcha hydrothermal vent snails. Mol. Biol. Evol. 37:12346984
    [Google Scholar]
  23. Breusing C, Osborn KJ, Girguis PR, Reese AT. 2022. Composition and metabolic potential of microbiomes associated with mesopelagic animals from Monterey Canyon. ISME Commun. 2:1117
    [Google Scholar]
  24. Bright M, Giere O. 2005. Microbial symbiosis in Annelida. Symbiosis 38:1145
    [Google Scholar]
  25. Bruijning M, Henry LP, Forsberg SKG, Metcalf CJE, Ayroles JF. 2022. Natural selection for imprecise vertical transmission in host-microbiota systems. Nat. Ecol. Evol. 6:17787
    [Google Scholar]
  26. Câmara Dos Reis M, Romac S, Le Gall F, Marie D, Frada MJ et al. 2022. Exploring the phycosphere of Emiliania huxleyi: from bloom dynamics to microbiome assembly experiments. Mol. Ecol. https://doi.org/10.1111/mec.16829
    [Google Scholar]
  27. Cavanaugh CM. 1994. Microbial symbiosis: patterns of diversity in the marine environment. Am. Zool. 34:17989
    [Google Scholar]
  28. Chauhan A, Singh R. 2019. Probiotics in aquaculture: a promising emerging alternative approach. Symbiosis 77:299113
    [Google Scholar]
  29. Conte C, Apostolaki ET, Vizzini S, Migliore L. 2023. A tight interaction between the native seagrass Cymodocea nodosaand the exotic Halophila stipulacea in the Aegean Sea highlights seagrass holobiont variations. Plants 12:2350
    [Google Scholar]
  30. Coyne KJ, Wang Y, Johnson G. 2022. Algicidal bacteria: a review of current knowledge and applications to control harmful algal blooms. Front. Microbiol. 13:871177
    [Google Scholar]
  31. Crump BC, Wojahn JM, Tomas F, Mueller RS. 2018. Metatranscriptomics and amplicon sequencing reveal mutualisms in seagrass microbiomes. Front. Microbiol. 9:388
    [Google Scholar]
  32. Daugherty MD, Malik HS. 2012. Rules of engagement: molecular insights from host-virus arms races. Annu. Rev. Genet. 46:677700
    [Google Scholar]
  33. Dawkins R. 2016. The Extended Phenotype: The Long Reach of the Gene Oxford, UK: Oxford Univ. Press
  34. de Vargas C, Audic S, Henry N, Decelle J, Mahé F et al. 2015. Eukaryotic plankton diversity in the sunlit ocean. Science 348:62371261605Describes the vast planktonic holobionts newly uncovered by Tara Oceans.
    [Google Scholar]
  35. Decelle J, Colin S, Foster RA 2015. Photosymbiosis in marine planktonic protists. Marine Protists: Diversity and Dynamics S Ohtsuka, T Suzaki, T Horiguchi, N Suzuki, F Not 465500. Tokyo: Springer
    [Google Scholar]
  36. Deck J, Gaither MR, Ewing R, Bird CE, Davies N et al. 2017. The Genomic Observatories Metadatabase (GeOMe): a new repository for field and sampling event metadata associated with genetic samples. PLOS Biol. 15:8e2002925
    [Google Scholar]
  37. Degnan SM. 2014. Think laterally: horizontal gene transfer from symbiotic microbes may extend the phenotype of marine sessile hosts. Front. Microbiol. 5:638
    [Google Scholar]
  38. Degnan SM, Degnan BM. 2010. The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution. Philos. Trans. R. Soc. Lond. B 365:154064151
    [Google Scholar]
  39. del Campo J, Bass D, Keeling PJ. 2020. The eukaryome: diversity and role of microeukaryotic organisms associated with animal hosts. Funct. Ecol. 34:10204554
    [Google Scholar]
  40. DeWeese KJ, Osborne MG. 2021. Understanding the metabolome and metagenome as extended phenotypes: the next frontier in macroalgae domestication and improvement. J. World Aquac. Soc. 52:5100930
    [Google Scholar]
  41. Dittami SM, Arboleda E, Auguet J-C, Bigalke A, Briand E et al. 2021. A community perspective on the concept of marine holobionts: current status, challenges, and future directions. PeerJ 9:e10911The first review on the state of research in marine holobionts.
    [Google Scholar]
  42. Djeghri N, Pondaven P, Le Grand F, Bideau A, Duquesne N et al. 2021. High trophic plasticity in the mixotrophic Mastigias papua-Symbiodiniaceae holobiont: implications for the ecology of zooxanthellate jellyfishes. Mar. Ecol. Prog. Ser. 666:7388
    [Google Scholar]
  43. Doolittle WF, Inkpen SA. 2018. Processes and patterns of interaction as units of selection: an introduction to ITSNTS thinking. PNAS 115:16400614
    [Google Scholar]
  44. Dror H, Novak L, Evans JS, López-Legentil S, Shenkar N. 2019. Core and dynamic microbial communities of two invasive ascidians: Can host-symbiont dynamics plasticity affect invasion capacity?. Microb. Ecol. 78:117084
    [Google Scholar]
  45. Eirin-Lopez JM, Putnam HM. 2019. Marine environmental epigenetics. Annu. Rev. Mar. Sci. 11:33568
    [Google Scholar]
  46. Espirito Santo ÉD, Ishii M, Pinto UM, Matsudo MC, Monteiro de Carvalho JC. 2022. Obtaining bioproducts from the studies of signals and interactions between microalgae and bacteria. Microorganisms 10:102029
    [Google Scholar]
  47. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:537423740
    [Google Scholar]
  48. Forterre P, Prangishvili D. 2013. The major role of viruses in cellular evolution: facts and hypotheses. Curr. Opin. Virol. 3:555865
    [Google Scholar]
  49. Freckelton ML, Nedved BT, Hadfield MG. 2017. Induction of invertebrate larval settlement; different bacteria, different mechanisms?. Sci. Rep. 7:142557
    [Google Scholar]
  50. Gilbert SF. 2019. Evolutionary transitions revisited: holobiont evo-devo. J. Exp. Zool. B 332:830714
    [Google Scholar]
  51. Glasl B, Bongaerts P, Elisabeth NH, Hoegh-Guldberg O, Herndl GJ, Frade PR. 2017. Microbiome variation in corals with distinct depth distribution ranges across a shallow-mesophotic gradient (15–85 m). Coral Reefs 36:244752
    [Google Scholar]
  52. González-Acosta B, Barraza A, Guadarrama-Analco C, Hernández-Guerrero CJ, Martínez-Díaz SF et al. 2022. Depth effect on the prokaryotic community assemblage associated with sponges from different rocky reefs. PeerJ 10:e13133
    [Google Scholar]
  53. González-Pech RA, Bhattacharya D, Ragan MA, Chan CX. 2019. Genome evolution of coral reef symbionts as intracellular residents. Trends Ecol. Evol. 34:9799806
    [Google Scholar]
  54. González-Pech RA, Stephens TG, Chen Y, Mohamed AR, Cheng Y et al. 2021. Comparison of 15 dinoflagellate genomes reveals extensive sequence and structural divergence in family Symbiodiniaceae and genus Symbiodinium. BMC Biol. 19:173
    [Google Scholar]
  55. Grasis JA. 2017. The intra-dependence of viruses and the holobiont. Front. Immunol. 8:1501
    [Google Scholar]
  56. Harvey EL, Deering RW, Rowley DC, El Gamal A, Schorn M et al. 2016. A bacterial quorum-sensing precursor induces mortality in the marine coccolithophore. Emiliania huxleyi. Front. Microbiol. 7:59
    [Google Scholar]
  57. Hauville MR, Zambonino-Infante JL, Gordon Bell J, Migaud H, Main KL 2016. Effects of a mix of Bacillus sp. as a potential probiotic for Florida pompano, common snook and red drum larvae performances and digestive enzyme activities. Aquac. Nutr. 22:15160
    [Google Scholar]
  58. Henry LP, Bruijning M, Forsberg SKG, Ayroles JF. 2021. The microbiome extends host evolutionary potential. Nat. Commun. 12:15141
    [Google Scholar]
  59. Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M et al. 2003. Microbial diversity of marine sponges. Prog. Mol. Subcell. Biol. 37:5988
    [Google Scholar]
  60. Hernandez-Agreda A, Leggat W, Bongaerts P, Herrera C, Ainsworth TD. 2018. Rethinking the coral microbiome: simplicity exists within a diverse microbial biosphere. mBio 9:5e00812-18
    [Google Scholar]
  61. Holt CC, Boscaro V, Van Steenkiste NWL, Herranz M, Mathur V et al. 2022. Microscopic marine invertebrates are reservoirs for cryptic and diverse protists and fungi. Microbiome 10:1161
    [Google Scholar]
  62. Ibarbalz FM, Henry N, Brandão MC, Martini S, Busseni G et al. 2019. Global trends in marine plankton diversity across kingdoms of life. Cell 179:5108497.e21
    [Google Scholar]
  63. Indraningrat AAG, Steinert G, Becking LE, Mueller B, de Goeij JM et al. 2022. Sponge holobionts shift their prokaryotic communities and antimicrobial activity from shallow to lower mesophotic depths. Antonie van Leeuwenhoek 115:10126583
    [Google Scholar]
  64. Irwin NAT, Pittis AA, Richards TA, Keeling PJ. 2022. Systematic evaluation of horizontal gene transfer between eukaryotes and viruses. Nat. Microbiol. 7:232736
    [Google Scholar]
  65. Jenkins BH, Maguire F, Leonard G, Eaton JD, West S et al. 2021. Emergent RNA-RNA interactions can promote stability in a facultative phototrophic endosymbiosis. PNAS 118:38e2108874118
    [Google Scholar]
  66. Jiang L, Sullivan H, Seligman C, Gilchrist S, Wang B. 2021. An NMR-based metabolomics study on sea anemones Exaiptasia diaphana (Rapp, 1829) with atrazine exposure. Mol. Omics 17:6101220
    [Google Scholar]
  67. Joint I, Tait K, Callow ME, Callow JA, Milton D et al. 2002. Cell-to-cell communication across the prokaryote-eukaryote boundary. Science 298:55961207
    [Google Scholar]
  68. Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC. 2012. Experimental evolution. Trends Ecol. Evol. 27:1054760
    [Google Scholar]
  69. Keeling PJ. 2009. Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr. Opin. Genet. Dev. 19:661319
    [Google Scholar]
  70. Koonin EV. 2016. Viruses and mobile elements as drivers of evolutionary transitions. Philos. Trans. R. Soc. Lond. B 371:170120150442
    [Google Scholar]
  71. Krishna Kumar R, Foster KR. 2023. 3D printing of microbial communities: a new platform for understanding and engineering microbiomes. Microb. Biotechnol.48993
    [Google Scholar]
  72. Kustra MC, Carrier TJ. 2022. On the spread of microbes that manipulate reproduction in marine invertebrates. Am. Nat. 200:221735
    [Google Scholar]
  73. Larsen T, Jefferson C, Bartley A, Strassmann JE, Queller DC. 2021. Inference of symbiotic adaptations in nature using experimental evolution. Evolution 75:494555
    [Google Scholar]
  74. Li S-N, Zhang C, Li F, Ren N-Q, Ho S-H. 2023. Recent advances of algae-bacteria consortia in aquatic remediation. Crit. Rev. Environ. Sci. Technol. 53:331539
    [Google Scholar]
  75. Lim SJ, Bordenstein SR. 2020. An introduction to phylosymbiosis. Proc. R. Soc. B 287:192220192900
    [Google Scholar]
  76. López-García P, Moreira D. 2020. The Syntrophy hypothesis for the origin of eukaryotes revisited. Nat. Microbiol. 5:565567
    [Google Scholar]
  77. Margulis L. 1991. Symbiogenesis and symbionticism. Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis L Margulis, R Fester 114. Cambridge, MA: MIT Press
    [Google Scholar]
  78. Marshall WL, Celio G, McLaughlin DJ, Berbee ML. 2008. Multiple isolations of a culturable, motile Ichthyosporean (Mesomycetozoa, Opisthokonta), Creolimax fragrantissima n. gen., n. sp., from marine invertebrate digestive tracts. Protist 159:341533
    [Google Scholar]
  79. Martin W, Russell MJ. 2003. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos. Trans. R. Soc. Lond. B 358:14295985
    [Google Scholar]
  80. McAnulty SJ, Kerwin AH, Koch E, Nuttall B, Suria AM et al. 2023.. “ Failure to launch”: development of a reproductive organ linked to symbiotic bacteria. mBio 14:1e02131-22
    [Google Scholar]
  81. McCutcheon JP, Moran NA. 2011. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10:11326
    [Google Scholar]
  82. McDaniel LD, Young E, Delaney J, Ruhnau F, Ritchie KB, Paul JH. 2010. High frequency of horizontal gene transfer in the oceans. Science 330:600050
    [Google Scholar]
  83. Medina M, Sachs JL. 2010. Symbiont genomics, our new tangled bank. Genomics 95:312937
    [Google Scholar]
  84. Medina M, Sharp V, Ohdera A, Bellantuono A, Dalrymple J et al. 2021. The upside-down jellyfish Cassiopea xamachana as an emerging model system to study cnidarian-algal symbiosis. Handbook of Marine Model Organisms in Experimental Biology: Established and Emerging A Boutet, B Schierwater 14971. Boca Raton, FL: CRC
    [Google Scholar]
  85. Mehrmohamadi M, Sepehri MH, Nazer N, Norouzi MR. 2021. A comparative overview of epigenomic profiling methods. Front. Cell Dev. Biol. 9:714687
    [Google Scholar]
  86. Miller MB, Bassler BL. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:16599
    [Google Scholar]
  87. Missawi O, Venditti M, Cappello T, Zitouni N, Marco GDE et al. 2022. Autophagic event and metabolomic disorders unveil cellular toxicity of environmental microplastics on marine polychaete Hediste diversicolor. Environ. Pollut. 302:119106
    [Google Scholar]
  88. Moreira D, López-García P. 1998. Symbiosis between methanogenic archaea and delta-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J. Mol. Evol. 47:551730
    [Google Scholar]
  89. Moriano-Gutierrez S, Ruby EG, McFall-Ngai MJ. 2021. MicroRNA-mediated regulation of initial host responses in a symbiotic organ. mSystems 6:3e00081-21
    [Google Scholar]
  90. Munday PL, Warner RR, Monro K, Pandolfi JM, Marshall DJ. 2013. Predicting evolutionary responses to climate change in the sea. Ecol. Lett. 16:121488500
    [Google Scholar]
  91. Musat N, Giere O, Gieseke A, Thiermann F, Amann R, Dubilier N. 2007. Molecular and morphological characterization of the association between bacterial endosymbionts and the marine nematode Astomonema sp. from the Bahamas. Environ. Microbiol. 9:5134553
    [Google Scholar]
  92. Muscatine L, Porter JW. 1977. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27:745460
    [Google Scholar]
  93. Needham DM, Poirier C, Bachy C, George EE, Wilken S et al. 2022. The microbiome of a bacterivorous marine choanoflagellate contains a resource-demanding obligate bacterial associate. Nat. Microbiol. 7:9146679
    [Google Scholar]
  94. Neu AT, Allen EE, Roy K. 2021. Defining and quantifying the core microbiome: challenges and prospects. PNAS 118:51e2104429118
    [Google Scholar]
  95. Nyholm SV, McFall-Ngai M. 2004. The winnowing: establishing the squid–Vibrio symbiosis. Nat. Rev. Microbiol. 2:863242
    [Google Scholar]
  96. O'Brien PA, Tan S, Yang C, Frade PR, Andreakis N et al. 2020. Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. ISME J. 14:9221122
    [Google Scholar]
  97. O'Brien PA, Webster NS, Miller DJ, Bourne DG. 2019. Host-microbe coevolution: applying evidence from model systems to complex marine invertebrate holobionts. mBio 10:1e02241-18
    [Google Scholar]
  98. Ohdera AH, Darymple J, Avila-Magaña V, Sharp V, Watson K et al. 2022. Symbiosis-driven development in an early branching metazoan. bioRxiv 2022.07.21.500558. https://doi.org/10.1101/2022.07.21.500558
  99. Oviedo JA, Muñoz R, Donoso-Bravo A, Bernard O, Casagli F, Jeison D. 2022. A half-century of research on microalgae-bacteria for wastewater treatment. Algal Res. 67:102828
    [Google Scholar]
  100. Palladino G, Rampelli S, Scicchitano D, Musella M, Quero GM et al. 2021. Impact of marine aquaculture on the microbiome associated with nearby holobionts: the case of Patella caerulea living in proximity of sea bream aquaculture cages. Microorganisms 9:2455
    [Google Scholar]
  101. Parkinson JE, Baums IB. 2014. The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front. Microbiol. 5:445
    [Google Scholar]
  102. Pawlowski J, Kelly-Quinn M, Altermatt F, Apothéloz-Perret-Gentil L, Beja P et al. 2018. The future of biotic indices in the ecogenomic era: integrating (e)DNA metabarcoding in biological assessment of aquatic ecosystems. Sci. Total Environ. 637–38:1295310
    [Google Scholar]
  103. Peixoto RS, Voolstra CR, Sweet M, Duarte CM, Carvalho S et al. 2022. Harnessing the microbiome to prevent global biodiversity loss. Nat. Microbiol. 7:11172635
    [Google Scholar]
  104. Pierce SK, Curtis NE, Middlebrooks ML. 2015. Sacoglossan sea slugs make routine use of photosynthesis by a variety of species-specific adaptations. Invertebr. Biol. 134:210315
    [Google Scholar]
  105. Pita L, Rix L, Slaby BM, Franke A, Hentschel U. 2018. The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6:46
    [Google Scholar]
  106. Poland DM, Mansfield JM, Hannes AR, Lewis CLF, Shearer TL et al. 2013. Variation in Symbiodinium communities in juvenile Briareum asbestinum (Cnidaria: Octocorallia) over temporal and spatial scales. Mar. Ecol. Prog. Ser. 476:2337
    [Google Scholar]
  107. Pollock FJ, McMinds R, Smith S, Bourne DG, Willis BL et al. 2018. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat. Commun. 9:14921
    [Google Scholar]
  108. Puntin G, Sweet M, Fraune S, Medina M, Sharp K et al. 2022. Harnessing the power of model organisms to unravel microbial functions in the coral holobiont. Microbiol. Mol. Biol. Rev. 86:4e00053-22
    [Google Scholar]
  109. Quigley KM, Willis BL, Bay LK. 2017. Heritability of the Symbiodinium community in vertically- and horizontally-transmitting broadcast spawning corals. Sci. Rep. 7:18219
    [Google Scholar]
  110. Raval PK, Garg SG, Gould SB. 2022. Endosymbiotic selective pressure at the origin of eukaryotic cell biology. eLife 11:e81033
    [Google Scholar]
  111. Richter DJ, Watteaux R, Vannier T, Leconte J, Frémont P et al. 2022. Genomic evidence for global ocean plankton biogeography shaped by large-scale current systems. eLife 11:e78129
    [Google Scholar]
  112. Rischer M, Guo H, Beemelmanns C. 2022. Signaling molecules inducing metamorphosis in marine organisms. Nat. Prod. Rep. 39:9183355
    [Google Scholar]
  113. Roughgarden J 2017. Model of holobiont population dynamics and evolution: a preliminary sketch. Landscapes of Collectivity in the Life Sciences SB Gissis, E Lamm, A Shavit 32550. Cambridge, MA: MIT Press
    [Google Scholar]
  114. Roughgarden J. 2023a. Holobiont evolution: population theory for the hologenome. Am. Nat. 201:676378Provides the first theoretical model of holobiont population genetics.
    [Google Scholar]
  115. Roughgarden J. 2023b. Population dynamics of the phage/bacteria interaction: “fitness switch” for lytic-lysogenic transition. bioRxiv 2023.01.03.522622. https://doi.org/10.1101/2023.01.03.522622
  116. Rypien KL, Baker DM. 2009. Isotopic labeling and antifungal resistance as tracers of gut passage of the sea fan pathogen Aspergillus sydowii. Dis. Aquat. Organ. 86:117
    [Google Scholar]
  117. Schuelke T, Pereira TJ, Hardy SM, Bik HM. 2018. Nematode-associated microbial taxa do not correlate with host phylogeny, geographic region or feeding morphology in marine sediment habitats. Mol. Ecol. 27:8193051
    [Google Scholar]
  118. Serra V, Gammuto L, Nitla V, Castelli M, Lanzoni O et al. 2020. Morphology, ultrastructure, genomics, and phylogeny of Euplotes vanleeuwenhoeki sp. nov. and its ultra-reduced endosymbiont “Candidatus Pinguicoccus supinus” sp. nov. Sci. Rep. 10:120311
    [Google Scholar]
  119. Seymour JR, Amin SA, Raina J-B, Stocker R. 2017. Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat. Microbiol. 2:717065Describes the role of the phycosphere in phytoplankton biology.
    [Google Scholar]
  120. Sharp C, Foster KR. 2022. Host control and the evolution of cooperation in host microbiomes. Nat. Commun. 13:13567
    [Google Scholar]
  121. Sharp KH, Ritchie KB, Schupp PJ, Ritson-Williams R, Paul VJ. 2010. Bacterial acquisition in juveniles of several broadcast spawning coral species. PLOS ONE 5:5e10898
    [Google Scholar]
  122. Shropshire JD, Bordenstein SR. 2016. Speciation by symbiosis: the microbiome and behavior. mBio 7:2e01785-15
    [Google Scholar]
  123. Singh RP, Baghel RS, Reddy CRK, Jha B. 2015. Effect of quorum sensing signals produced by seaweed-associated bacteria on carpospore liberation from Gracilaria dura. Front. Plant Sci. 6:117
    [Google Scholar]
  124. Singh RP, Reddy CRK. 2015. Unraveling the functions of the macroalgal microbiome. Front. Microbiol. 6:1488
    [Google Scholar]
  125. Skinner C, Cobain MRD, Zhu Y, Wyatt ASJ, Polunin NVC 2022. Progress and direction in the use of stable isotopes to understand complex coral reef ecosystems: a review. Oceanography and Marine Biology: An Annual Review, Vol. 60 SJ Hawkins, AL Allcock, AE Bates, M Byrne, AJ Evans, et al. 373432. Boca Raton, FL: CRC
    [Google Scholar]
  126. Sneed JM, Sharp KH, Ritchie KB, Paul VJ. 2014. The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals. Proc. R. Soc. B 281:178620133086
    [Google Scholar]
  127. Sogin EM, Kleiner M, Borowski C, Gruber-Vodicka HR, Dubilier N. 2021. Life in the dark: phylogenetic and physiological diversity of chemosynthetic symbioses. Annu. Rev. Microbiol. 75:695718
    [Google Scholar]
  128. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM et al. 2006. Microbial diversity in the deep sea and the underexplored “rare biosphere. .” PNAS 103:321211520
    [Google Scholar]
  129. Song H, Hewitt OH, Degnan SM. 2021. Arginine biosynthesis by a bacterial symbiont enables nitric oxide production and facilitates larval settlement in the marine-sponge host. Curr. Biol. 31:243337.e3
    [Google Scholar]
  130. Stévenne C, Micha M, Plumier J-C, Roberty S. 2021. Corals and sponges under the light of the holobiont concept: how microbiomes underpin our understanding of marine ecosystems. Front. Mar. Sci. 8:698853
    [Google Scholar]
  131. Sunagawa S, Woodley CM, Medina M. 2010. Threatened corals provide underexplored microbial habitats. PLOS ONE 5:3e9554
    [Google Scholar]
  132. Takagi H, Kimoto K, Fujiki T, Moriya K. 2018. Effect of nutritional condition on photosymbiotic consortium of cultured Globigerinoides sacculifer (Rhizaria, Foraminifera). Symbiosis 76:12539
    [Google Scholar]
  133. Tarnecki AM, Wafapoor M, Phillips RN, Rhody NR. 2019. Benefits of a Bacillus probiotic to larval fish survival and transport stress resistance. Sci. Rep. 9:14892
    [Google Scholar]
  134. Thompson JR, Rivera HE, Closek CJ, Medina M. 2014. Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front. Cell. Infect. Microbiol. 4:176
    [Google Scholar]
  135. Uwizeye C, Mars Brisbin M, Gallet B, Chevalier F, LeKieffre C et al. 2021. Cytoklepty in the plankton: a host strategy to optimize the bioenergetic machinery of endosymbiotic algae. PNAS 118:27e2025252118
    [Google Scholar]
  136. van der Loos LM, Eriksson BK, Falcão Salles J. 2019. The macroalgal holobiont in a changing sea. Trends Microbiol. 27:763550
    [Google Scholar]
  137. Van Etten J, Bhattacharya D. 2020. Horizontal gene transfer in eukaryotes: not if, but how much?. Trends Genet. 36:1291525
    [Google Scholar]
  138. van Oppen MJH, Blackall LL. 2019. Coral microbiome dynamics, functions and design in a changing world. Nat. Rev. Microbiol. 17:955767
    [Google Scholar]
  139. Verma SC, Miyashiro T. 2013. Quorum sensing in the squid-Vibrio symbiosis. Int. J. Mol. Sci. 14:816386401
    [Google Scholar]
  140. Voolstra CR, Suggett DJ, Peixoto RS, Parkinson JE, Quigley KM et al. 2021. Extending the natural adaptive capacity of coral holobionts. Nat. Rev. Earth Environ. 2:1174762
    [Google Scholar]
  141. Wang R, Sun R, Zhang Z, Vannini C, Di Giuseppe G, Liang A. 2022.. “ Candidatus Euplotechlamydia quinta,” a novel Chlamydia-like bacterium hosted by the ciliate Euplotes octocarinatus (Ciliophora, Spirotrichea). J. Eukaryot. Microbiol. 70:2e12945
    [Google Scholar]
  142. Wang Y, Zhao Y, Bollas A, Wang Y, Au KF. 2021. Nanopore sequencing technology, bioinformatics and applications. Nat. Biotechnol. 39:11134865
    [Google Scholar]
  143. Webster NS, Botté ES, Soo RM, Whalan S. 2011. The larval sponge holobiont exhibits high thermal tolerance. Environ. Microbiol. Rep. 3:675662
    [Google Scholar]
  144. Whalen KE, Kirby C, Nicholson RM, O'Reilly M, Moore BS, Harvey EL 2018. The chemical cue tetrabromopyrrole induces rapid cellular stress and mortality in phytoplankton. Sci. Rep. 8:115498
    [Google Scholar]
  145. Wichard T. 2023. From model organism to application: bacteria-induced growth and development of the green seaweed Ulva and the potential of microbe leveraging in algal aquaculture. Semin. Cell Dev. Biol. 134:6978
    [Google Scholar]
  146. Woznica A, Cantley AM, Beemelmanns C, Freinkman E, Clardy J, King N. 2016. Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates. PNAS 113:28789499
    [Google Scholar]
  147. Woznica A, Gerdt JP, Hulett RE, Clardy J, King N. 2017. Mating in the closest living relatives of animals is induced by a bacterial chondroitinase. Cell 170:6117583.e11
    [Google Scholar]
  148. Yao S, Lyu S, An Y, Lu J, Gjermansen C, Schramm A. 2019. Microalgae-bacteria symbiosis in microalgal growth and biofuel production: a review. J. Appl. Microbiol. 126:235968
    [Google Scholar]
  149. Yarden O, Ainsworth TD, Roff G, Leggat W, Fine M, Hoegh-Guldberg O. 2007. Increased prevalence of ubiquitous ascomycetes in an acroporid coral (Acropora formosa) exhibiting symptoms of brown band syndrome and skeletal eroding band disease. Appl. Environ. Microbiol. 73:8275557
    [Google Scholar]
  150. Zhang H-H, Peccoud J, Xu M-R-X, Zhang X-G, Gilbert C. 2020. Horizontal transfer and evolution of transposable elements in vertebrates. Nat. Commun. 11:11362
    [Google Scholar]
  151. Zhao L, Zhang H, Kohnen MV, Prasad KVSK, Gu L, Reddy ASN. 2019. Analysis of transcriptome and epitranscriptome in plants using PacBio Iso-Seq and nanopore-based direct RNA sequencing. Front. Genet. 10:253
    [Google Scholar]
  152. Zilber-Rosenberg I, Rosenberg E. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32:572335Introduces the hologenome concept.
    [Google Scholar]
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