1932

Abstract

Microbial communities associated with deep-sea animals are critical to the establishment of novel biological communities in unusual environments. Over the past few decades, rapid exploration of the deep sea has enabled the discovery of novel microbial communities, some of which form symbiotic relationships with animal hosts. Symbiosis in the deep sea changes host physiology, behavior, ecology, and evolution over time and space. Symbiont diversity within a host is often aligned with diverse metabolic pathways that broaden the environmental niche for the animal host. In this review, we focus on microbiomes and obligate symbionts found in different deep-sea habitats and how they facilitate survival of the organisms that live in these environments. In addition, we discuss factors that govern microbiome diversity, host specificity, and biogeography in the deep sea. Finally, we highlight the current limitations of microbiome research and draw a road map for future directions to advance our knowledge of microbiomes in the deep sea.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-081621-112021
2022-02-15
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/animal/10/1/annurev-animal-081621-112021.html?itemId=/content/journals/10.1146/annurev-animal-081621-112021&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Bang C, Dagan T, Deines P, Dubilier N, Duschl WJ et al. 2018. Metaorganisms in extreme environments: Do microbes play a role in organismal adaptation?. Zoology 127:1–19
    [Google Scholar]
  2. 2. 
    Sogin EM, Leisch N, Dubilier N. 2020. Chemosynthetic symbioses. Curr. Biol. 30:R1137–42
    [Google Scholar]
  3. 3. 
    Bergin C, Wentrup C, Brewig N, Blazejak A, Erséuz C et al. 2018. Acquisition of a novel sulfur-oxidizing symbiont in the gutless marine worm Inanidrilus exumae. Appl. Environ. Microbiol. 84:e02267-17
    [Google Scholar]
  4. 4. 
    Childress JJ, Fisher CR, Brooks JM, Kennicutt MC2nd, Bidigare R, Anderson AE 1986. A methanotrophic marine molluscan (Bivalvia, mytilidae) symbiosis: mussels fueled by gas. Science 233:1306–8
    [Google Scholar]
  5. 5. 
    Widder EA. 2010. Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity. Science 328:704–8
    [Google Scholar]
  6. 6. 
    Rouse GW, Wilson NG, Worsaae K, Vrijenhoek RC 2015. A dwarf male reversal in bone-eating worms. Curr. Biol. 25:236–41
    [Google Scholar]
  7. 7. 
    Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T et al. 2005. Evolutionary innovation: a bone-eating marine symbiosis. Environ. Microbiol. 7:1369–78
    [Google Scholar]
  8. 8. 
    Smith CR, Glover AG, Treude T, Higgs ND, Amon DJ. 2015. Whale-fall ecosystems: recent insights into ecology, paleoecology, and evolution. Annu. Rev. Mar. Sci. 7:571–96
    [Google Scholar]
  9. 9. 
    Beinart RA, Sanders JG, Faure B, Sylva SP, Lee RW et al. 2012. Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses. PNAS 109:E3241–50
    [Google Scholar]
  10. 10. 
    Ip JC-H, Xu T, Sun J, Li R, Chen C et al. 2021. Host-endosymbiont genome integration in a deep-sea chemosymbiotic clam. Mol. Biol. Evol. 38:502–18
    [Google Scholar]
  11. 11. 
    Ansorge R, Romano S, Sayavedra L, González Porras MA, Kupczok A et al. 2019. Functional diversity enables multiple symbiont strains to coexist in deep-sea mussels. Nat. Microbiol. 4:2487–97
    [Google Scholar]
  12. 12. 
    Wilkins LGE, Leray M, O'Dea A, Yuen B, Peixoto RS et al. 2019. Host-associated microbiomes drive structure and function of marine ecosystems. PLOS Biol. 17:e3000533
    [Google Scholar]
  13. 13. 
    Vohsen SA, Gruber-Vodicka HR, Osman EO, Saxton MA, Joye SB et al. 2020. Deep-sea corals near cold seeps associate with chemoautotrophic bacteria that are related to the symbionts of cold seep and hydrothermal vent mussels. bioRxiv. 958453. https://doi.org/10.1101/2020.02.27.968453
    [Crossref]
  14. 14. 
    Goffredi SK, Motooka C, Fike DA, Gusmão LC, Tilic E et al. 2021. Mixotrophic chemosynthesis in a deep-sea anemone from hydrothermal vents in the Pescadero Basin, Gulf of California. BMC Biol 19:8
    [Google Scholar]
  15. 15. 
    Peixoto RS, Harkins DM, Nelson KE. 2021. Advances in microbiome research for animal health. Annu. Rev. Anim. Biosci. 9:289–311
    [Google Scholar]
  16. 16. 
    Kennedy J, Flemer B, Jackson SA, Morrissey JP, O'Gara F et al. 2014. Evidence of a putative deep sea specific microbiome in marine sponges. PLOS ONE 9:e91092
    [Google Scholar]
  17. 17. 
    Aronson HS, Zellmer AJ, Goffredi SK. 2017. The specific and exclusive microbiome of the deep-sea bone-eating snail, Rubyspira osteovora. FEMS Microbiol. Ecol. 93:fiw250
    [Google Scholar]
  18. 18. 
    Zhang N, Song C, Wang M, Liu Y, Hui M, Cui Z 2017. Diversity and characterization of bacteria associated with the deep-sea hydrothermal vent crab Austinograea sp. comparing with those of two shallow-water crabs by 16S ribosomal DNA analysis. PLOS ONE 12:e0187842
    [Google Scholar]
  19. 19. 
    Ohwada K, Tabor PS, Colwell RR. 1980. Species composition and barotolerance of gut microflora of deep-sea benthic macrofauna collected at various depths in the Atlantic Ocean. Appl. Environ. Microbiol. 40:746–55
    [Google Scholar]
  20. 20. 
    Collins FWJ, Walsh CJ, Gomez-Sala B, Guijarro-García E, Stokes D et al. 2021. The microbiome of deep-sea fish reveals new microbial species and a sparsity of antibiotic resistance genes. Gut Microbes 13:1921924
    [Google Scholar]
  21. 21. 
    Lian CA, Zhu FC, Wei ZF, He LS 2021. Composition and potential functions of the dominant microbiota in deep-sea hagfish gut from the South China Sea. Deep Sea Res. I 169:103488
    [Google Scholar]
  22. 22. 
    Wang Y, Huang J-M, Wang S-L, Gao Z-M, Zhang A-Q et al. 2016. Genomic characterization of symbiotic mycoplasmas from the stomach of deep-sea isopod Bathynomus sp. Environ. Microbiol. 18:2646–59
    [Google Scholar]
  23. 23. 
    Corbari L, Durand L, Cambon-Bonavita MA, Gaill F, Compère P 2012. New digestive symbiosis in the hydrothermal vent amphipoda Ventiella sulfuris. C. R. Biol. 335:142–54
    [Google Scholar]
  24. 24. 
    Liu H, Guo X, Gooneratne R, Lai R, Zeng C et al. 2016. The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels. Sci. Rep. 6:24340
    [Google Scholar]
  25. 25. 
    Ngugi DK, Miyake S, Cahill M, Vinu M, Hackmann TJ et al. 2017. Genomic diversification of giant enteric symbionts reflects host dietary lifestyles. PNAS 114:E7592–601
    [Google Scholar]
  26. 26. 
    Galand PE, Remize M, Meistertzheim A-L, Pruski AM, Peru E et al. 2020. Diet shapes cold-water corals bacterial communities. Environ. Microbiol. 22:354–68
    [Google Scholar]
  27. 27. 
    Röthig T, Roik A, Yum LK, Voolstra CR. 2017. Distinct bacterial microbiomes associate with the deep-sea coral Eguchipsammia fistula from the Red Sea and from aquaria settings. Front. Mar. Sci. 4:259
    [Google Scholar]
  28. 28. 
    Röthig T, Yum LK, Kremb SG, Roik A, Voolstra CR 2017. Microbial community composition of deep-sea corals from the Red Sea provides insight into functional adaption to a unique environment. Sci. Rep. 7:44714
    [Google Scholar]
  29. 29. 
    Galand PE, Chapron L, Meistertzheim A-L, Peru E, Lartaud F 2018. The effect of captivity on the dynamics of active bacterial communities differs between two deep-sea coral species. Front. Microbiol. 9:2565
    [Google Scholar]
  30. 30. 
    Kellogg CA. 2019. Microbiomes of stony and soft deep-sea corals share rare core bacteria. Microbiome 7:90
    [Google Scholar]
  31. 31. 
    Osman EO, Suggett DJ, Voolstra CR, Pettay DT, Clark DR et al. 2020. Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities. Microbiome 8:8
    [Google Scholar]
  32. 32. 
    van de Water JAJM, Allemand D, Ferrier-Pagès C. 2018. Host-microbe interactions in octocoral holobionts—recent advances and perspectives. Microbiome 6:64
    [Google Scholar]
  33. 33. 
    Cheng XY, Wang Y, Li JY, Yan GY, He LS 2019. Comparative analysis of the gut microbial communities between two dominant amphipods from the Challenger Deep, Mariana Trench. Deep Sea Res. I 151:103081
    [Google Scholar]
  34. 34. 
    Talwar C, Nagar S, Lal R, Negi RK. 2018. Fish gut microbiome: current approaches and future perspectives. Indian J. Microbiol. 58:397–414
    [Google Scholar]
  35. 35. 
    Verhoeven JTP, Kavanagh AN, Dufour SC. 2017. Microbiome analysis shows enrichment for specific bacteria in separate anatomical regions of the deep-sea carnivorous sponge Chondrocladia grandis. FEMS Microbiol. Ecol. 93:fiw214
    [Google Scholar]
  36. 36. 
    Weiler BA, Verhoeven JTP, Dufour SC. 2018. Bacterial communities in tissues and surficial mucus of the cold-water coral Paragorgia arborea. Front. Mar. Sci. 5:378
    [Google Scholar]
  37. 37. 
    Pollock FJ, McMinds R, Smith S, Bourne DG, Willis BL et al. 2018. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat. Commun. 9:4921
    [Google Scholar]
  38. 38. 
    O'Brien PA, Tan S, Yang C, Frade PR, Andreakis N et al. 2020. Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. ISME J 14:2211–22
    [Google Scholar]
  39. 39. 
    Tang Y, Ma KY, Cheung MK, Yang C-H, Wang Y et al. 2021. Gut microbiota in decapod shrimps: evidence of phylosymbiosis. Microb. Ecol. 82:994–1007
    [Google Scholar]
  40. 40. 
    Chiarello M, Auguet J-C, Bettarel Y, Bouvier C, Claverie T et al. 2018. Skin microbiome of coral reef fish is highly variable and driven by host phylogeny and diet. Microbiome 6:147
    [Google Scholar]
  41. 41. 
    Kohl KD, Dearing MD, Bordenstein SR. 2018. Microbial communities exhibit host species distinguishability and phylosymbiosis along the length of the gastrointestinal tract. Mol. Ecol. 27:1874–83
    [Google Scholar]
  42. 42. 
    Brooks AW, Kohl KD, Brucker RM, van Opstal EJ, Bordenstein SR. 2016. Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLOS Biol 14:e2000225
    [Google Scholar]
  43. 43. 
    Lim SJ, Bordenstein SR. 2020. An introduction to phylosymbiosis. Proc. R. Soc. B 287:20192900
    [Google Scholar]
  44. 44. 
    Ainsworth TD, Krause L, Bridge T, Torda G, Raina J-B et al. 2015. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9:2261–74
    [Google Scholar]
  45. 45. 
    Hernandez-Agreda A, Leggat W, Bongaerts P, Ainsworth TD. 2016. The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. mBio 7: e00560-16
    [Google Scholar]
  46. 46. 
    Polz MF, Cavanaugh CM. 1995. Dominance of one bacterial phylotype at a Mid-Atlantic Ridge hydrothermal vent site. PNAS 92:7232–36
    [Google Scholar]
  47. 47. 
    Haddad A, Camacho F, Durand P, Cary SC 1995. Phylogenetic characterization of the epibiotic bacteria associated with the hydrothermal vent polychaete Alvinella pompejana. Appl. Environ. Microbiol. 61:1679–87
    [Google Scholar]
  48. 48. 
    Urakawa H, Dubilier N, Fujiwara Y, Cunningham DE, Kojima S, Stahl DA 2005. Hydrothermal vent gastropods from the same family (Provannidae) harbour ε- and γ-proteobacterial endosymbionts. Environ. Microbiol. 7:750–54
    [Google Scholar]
  49. 49. 
    Nakagawa S, Takai K. 2008. Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol. Ecol. 65:1–14
    [Google Scholar]
  50. 50. 
    Dubilier N, Bergin C, Lott C. 2008. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6:725–40
    [Google Scholar]
  51. 51. 
    Blazejak A, Kuever J, Erséus C, Amann R, Dubilier N 2006. Phylogeny of 16S rRNA, ribulose 1,5-bisphosphate carboxylase/oxygenase, and adenosine 5′-phosphosulfate reductase genes from gamma- and alphaproteobacterial symbionts in gutless marine worms (oligochaeta) from Bermuda and the Bahamas. Appl. Environ. Microbiol. 72:5527–36
    [Google Scholar]
  52. 52. 
    Fisher CR, Brooks JM, Vodenichar JS, Zande JM, Childress JJ, Burke RA Jr. 1993. The co-occurrence of methanotrophic and chemoautotrophic sulfur-oxidizing bacterial symbionts in a deep-sea mussel. Mar. Ecol. 14:277–89
    [Google Scholar]
  53. 53. 
    Brodl E, Winkler A, Macheroux P. 2018. Molecular mechanisms of bacterial bioluminescence. Comput. Struct. Biotechnol. J. 16:551–64
    [Google Scholar]
  54. 54. 
    Belas R, Mileham A, Cohn D, Hilman M, Simon M, Silverman M 1982. Bacterial bioluminescence: isolation and expression of the luciferase genes from Vibrio harveyi. Science 218:791–93
    [Google Scholar]
  55. 55. 
    Nealson KH, Hastings JW 2006. Quorum sensing on a global scale: Massive numbers of bioluminescent bacteria make milky seas. Appl. Environ. Microbiol. 72:2295–97
    [Google Scholar]
  56. 56. 
    Chakrabarty P, Davis MP, Smith WL, Baldwin ZH, Sparks JS. 2011. Is sexual selection driving diversification of the bioluminescent ponyfishes (Teleostei: Leiognathidae)?. Mol. Ecol. 20:2818–34
    [Google Scholar]
  57. 57. 
    Chakrabarty P, Davis MP, Smith WL, Berquist R, Gledhill KM et al. 2011. Evolution of the light organ system in ponyfishes (Teleostei: Leiognathidae). J. Morphol. 272:704–21
    [Google Scholar]
  58. 58. 
    Dunlap PV, Urbanczyk H 2013. Luminous bacteria. The Prokaryotes: Prokaryotic Physiology and Biochemistry E Rosenberg, EF DeLong, E Stackebrandt, S Lory, F Thompson 863–92 Berlin: Springer-Verlag
    [Google Scholar]
  59. 59. 
    Hendry TA, de Wet JR, Dougan KE, Dunlap PV. 2016. Genome evolution in the obligate but environmentally active luminous symbionts of flashlight fish. Genome Biol. Evol. 8:2203–13
    [Google Scholar]
  60. 60. 
    Vannier T, Hingamp P, Turrel F, Tanet L, Lescot M, Timsit Y. 2020. Diversity and evolution of bacterial bioluminescence genes in the global ocean. NAR Genom. Bioinform. 2:lqaa018
    [Google Scholar]
  61. 61. 
    Zielinski FU, Pernthaler A, Duperron S, Raggi L, Giere O et al. 2009. Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels. Environ. Microbiol. 11:1150–67
    [Google Scholar]
  62. 62. 
    Beinart RA, Nyholm SV, Dubilier N, Girguis PR. 2014. Intracellular Oceanospirillales inhabit the gills of the hydrothermal vent snail Alviniconcha with chemosynthetic, γ-proteobacterial symbionts. Environ. Microbiol. Rep. 6:656–64
    [Google Scholar]
  63. 63. 
    Terlizzi CM, Ward ME, Van Dover CL. 2004. Observations on parasitism in deep-sea hydrothermal vent and seep limpets. Dis. Aquat. Organ. 62:17–26
    [Google Scholar]
  64. 64. 
    Ward ME, Shields JD, Van Dover CL. 2004. Parasitism in species of Bathymodiolus (Bivalvia: Mytilidae) mussels from deep-sea seep and hydrothermal vents. Dis. Aquat. Organ. 62:1–16
    [Google Scholar]
  65. 65. 
    Sapir A, Dillman AR, Connon SA, Grupe BM, Ingels J et al. 2014. Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea. Front. Microbiol. 5:43
    [Google Scholar]
  66. 66. 
    Neulinger SC, Gärtner A, Järnegren J, Ludvigsen M, Lochte K et al. 2009. Tissue-associated “Candidatus Mycoplasma corallicola” and filamentous bacteria on the cold-water coral Lophelia pertusa (Scleractinia). Appl. Environ. Microbiol. 75:1437–44
    [Google Scholar]
  67. 67. 
    Gray MA, Stone RP, McLaughlin MR, Kellogg CA. 2011. Microbial consortia of gorgonian corals from the Aleutian islands. FEMS Microbiol. Ecol. 76:109–20
    [Google Scholar]
  68. 68. 
    van de Water JAJM, Voolstra CR, Rottier C, Cocito S, Peirano A et al. 2018. Seasonal stability in the microbiomes of temperate gorgonians and the red coral Corallium rubrum across the Mediterranean Sea. Microb. Ecol. 75:274–88
    [Google Scholar]
  69. 69. 
    van de Water JAJM, Melkonian R, Voolstra CR, Junca H, Beraud E et al. 2017. Comparative assessment of Mediterranean gorgonian-associated microbial communities reveals conserved core and locally variant bacteria. Microb. Ecol. 73:466–78
    [Google Scholar]
  70. 70. 
    Le Roux F, Goubet A, Thompson FL, Faury N, Gay M et al. 2005. Vibrio gigantis sp. nov., isolated from the haemolymph of cultured oysters (Crassostrea gigas). Int. J. Syst. Evol. Microbiol. 55:2251–55
    [Google Scholar]
  71. 71. 
    Beleneva IA, Kukhlevskii AD. 2010. Characterization of Vibrio gigantis and Vibrio pomeroyi isolated from invertebrates of Peter the Great Bay, Sea of Japan. Microbiology 79:402–7
    [Google Scholar]
  72. 72. 
    Franco T, Califano G, Gonçalves ACS, Cúcio C, Costa R 2016. Draft genome sequence of Vibrio sp. strain Evh12, a bacterium retrieved from the gorgonian coral Eunicella verrucosa. Genome Announc 4:e01729-15
    [Google Scholar]
  73. 73. 
    Vohsen SA, Anderson KE, Gade AM, Gruber-Vodicka HR, Dannenberg RP et al. 2020. Deep-sea corals provide new insight into the ecology, evolution, and the role of plastids in widespread apicomplexan symbionts of anthozoans. Microbiome 8:34
    [Google Scholar]
  74. 74. 
    Watsuji TO, Yamamoto A, Matoki K, Ueda K, Hada E et al. 2015. Molecular evidence of digestion and absorption of epibiotic bacterial community by deep-sea crab Shinkaia crosnieri. ISME J. 9:821–31
    [Google Scholar]
  75. 75. 
    Gardebrecht A, Markert S, Sievert SM, Felbeck H, Thürmer A et al. 2012. Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics. ISME J. 6:766–76
    [Google Scholar]
  76. 76. 
    Sayavedra L, Kleiner M, Ponnudurai R, Wetzel S, Pelletier E et al. 2015. Abundant toxin-related genes in the genomes of beneficial symbionts from deep-sea hydrothermal vent mussels. eLife 4:e07966
    [Google Scholar]
  77. 77. 
    Goffredi SK, Warén A, Orphan VJ, Van Dover CL, Vrijenhoek RC. 2004. Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Appl. Environ. Microbiol. 70:3082–90
    [Google Scholar]
  78. 78. 
    Baker LJ, Freed LL, Easson CG, Lopez JV, Fenolio D et al. 2019. Diverse deep-sea anglerfishes share a genetically reduced luminous symbiont that is acquired from the environment. eLife 8:e47606
    [Google Scholar]
  79. 79. 
    McCutcheon JP, Moran NA. 2012. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10:13–26
    [Google Scholar]
  80. 80. 
    Jäckle O, Seah BKB, Tietjen M, Leisch N, Liebek M et al. 2019. Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm Paracatenula. PNAS 116:8505–14
    [Google Scholar]
  81. 81. 
    Hendry TA, Freed LL, Fader D, Fenolio D, Sutton TT, Lopez JV 2018. Ongoing transposon-mediated genome reduction in the luminous bacterial symbionts of deep-sea ceratioid anglerfishes. mBio 9:e01033-18
    [Google Scholar]
  82. 82. 
    Duperron S, Nadalig T, Caprais J-C, Sibuet M, Fiala-Médioni A et al. 2005. Dual symbiosis in a Bathymodiolus sp. mussel from a methane seep on the Gabon Continental Margin (Southeast Atlantic): 16S rRNA phylogeny and distribution of the symbionts in gills. Appl. Environ. Microbiol. 71:1694–700
    [Google Scholar]
  83. 83. 
    Fujiwaral Y, Kawato M, Noda C, Kinoshita G, Yamanaka T et al. 2010. Extracellular and mixotrophic symbiosis in the whale-fall mussel Adipicola pacifica: a trend in evolution from extra- to intracellular symbiosis. PLOS ONE 5:e11808
    [Google Scholar]
  84. 84. 
    Baco AR, Smith CR, Peek AS, Roderick GK, Vrijenhoek RC. 1999. The phylogenetic relationships of whale-fall vesicomyid clams based on mitochondrial COI DNA sequences. Mar. Ecol. Prog. Ser. 182:137–47
    [Google Scholar]
  85. 85. 
    Feldman RA, Shank TM, Black MB, Baco AR, Smith CR, Vrijenhoek RC. 1998. Vestimentiferan on a whale fall. Biol. Bull. 194:116–19
    [Google Scholar]
  86. 86. 
    Petersen JM, Wentrup C, Verna C, Knittel K, Dubilier N. 2012. Origins and evolutionary flexibility of chemosynthetic symbionts from deep-sea animals. Biol. Bull. 223:123–37
    [Google Scholar]
  87. 87. 
    Duperron S, Sibuet M, MacGregor BJ, Kuypers MMM, Fisher CR, Dubilier N. 2007. Diversity, relative abundance and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussel species from cold seeps in the Gulf of Mexico. Environ. Microbiol. 9:1423–38
    [Google Scholar]
  88. 88. 
    Blazejak A, Erséus C, Amann R, Dubilier N 2005. Coexistence of bacterial sulfide oxidizers, sulfate reducers, and spirochetes in a gutless worm (oligochaeta) from the Peru margin. Appl. Environ. Microbiol. 71:1553–61
    [Google Scholar]
  89. 89. 
    Ruehland C, Blazejak A, Lott C, Loy A, Erséus C, Dubilier N. 2008. Multiple bacterial symbionts in two species of co-occurring gutless oligochaete worms from Mediterranean sea grass sediments. Environ. Microbiol. 10:3404–16
    [Google Scholar]
  90. 90. 
    Dubilier N, Mülders C, Ferdelman T, de Beer D, Pernthaler A et al. 2001. Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411:298–302
    [Google Scholar]
  91. 91. 
    Kleiner M, Wentrup C, Lott C, Teeling H, Wetzel S et al. 2012. Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use. PNAS 109:E1173–82
    [Google Scholar]
  92. 92. 
    Stewart FJ, Young CR, Cavanaugh CM. 2008. Lateral symbiont acquisition in a maternally transmitted chemosynthetic clam endosymbiosis. Mol. Biol. Evol. 25:673–87
    [Google Scholar]
  93. 93. 
    Decker C, Olu K, Arnaud-Haond S, Duperron S. 2013. Physical proximity may promote lateral acquisition of bacterial symbionts in vesicomyid clams. PLOS ONE 8:e64830
    [Google Scholar]
  94. 94. 
    Ebert D. 2013. The epidemiology and evolution of symbionts with mixed-mode transmission. Annu. Rev. Ecol. Evol. Syst. 44:623–43
    [Google Scholar]
  95. 95. 
    Russell SL, Corbett-Detig RB, Cavanaugh CM. 2017. Mixed transmission modes and dynamic genome evolution in an obligate animal-bacterial symbiosis. ISME J. 11:1359–71
    [Google Scholar]
  96. 96. 
    Schwartzman JA, Ruby EG. 2016. A conserved chemical dialog of mutualism: lessons from squid and vibrio. Microbes Infect. 18:1–10
    [Google Scholar]
  97. 97. 
    Suzuki Y, Kojima S, Watanabe HK, Suzuki M, Tsuchida S et al. 2006. Single host and symbiont lineages of hydrothermal-vent gastropods Ifremeria nautilei (Provannidae): biogeography and evolution. Mar. Ecol. Prog. Ser. 315:167–75
    [Google Scholar]
  98. 98. 
    Osvatic JT, Wilkins LGE, Leibrecht L, Leray M, Zauner S et al. 2021. Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups. PNAS 118:e2104378118
    [Google Scholar]
  99. 99. 
    Beinart RA, Luo C, Konstantinidis KT, Stewart FJ, Girguis PR. 2019. The bacterial symbionts of closely related hydrothermal vent snails with distinct geochemical habitats show broad similarity in chemoautotrophic gene content. Front. Microbiol. 10:1818
    [Google Scholar]
  100. 100. 
    Nussbaumer AD, Fisher CR, Bright M. 2006. Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441:345–48
    [Google Scholar]
  101. 101. 
    Perez M, Juniper SK. 2016. Insights into symbiont population structure among three vestimentiferan tubeworm host species at eastern Pacific spreading centers. Appl. Environ. Microbiol. 82:5197–205
    [Google Scholar]
  102. 102. 
    Romero Picazo D, Dagan T, Ansorge R, Petersen JM, Dubilier N, Kupczok A. 2019. Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated. ISME J 13:2954–68
    [Google Scholar]
  103. 103. 
    Munk O, Herring PJ. 1996. An early stage in development of escae and caruncles in the deep-sea anglerfish Cryptopsaras couesi (Pisces: Ceratioidei). J. Mar. Biol. Assoc. UK 76:517–27
    [Google Scholar]
  104. 104. 
    Freed LL, Easson C, Baker LJ, Fenolio D, Sutton TT et al. 2019. Characterization of the microbiome and bioluminescent symbionts across life stages of Ceratioid Anglerfishes of the Gulf of Mexico. FEMS Microbiol. Ecol. 95:fiz146
    [Google Scholar]
  105. 105. 
    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
    [Google Scholar]
  106. 106. 
    Davy SK, Allemand D, Weis VM 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76:229–61
    [Google Scholar]
  107. 107. 
    Mandel MJ, Schaefer AL, Brennan CA, Heath-Heckman EAC, Deloney-Marino CR et al. 2012. Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl. Environ. Microbiol. 78:4620–26
    [Google Scholar]
  108. 108. 
    Vohsen SA, Fisher CR, Baums IB. 2019. Metabolomic richness and fingerprints of deep-sea coral species and populations. Metabolomics 15:34
    [Google Scholar]
  109. 109. 
    Imbs AB, Demidkova DA, Dautova TN, Latyshev NA. 2009. Fatty acid biomarkers of symbionts and unusual inhibition of tetracosapolyenoic acid biosynthesis in corals (Octocorallia). Lipids 44:325–35
    [Google Scholar]
  110. 110. 
    Sogin EM, Putnam HM, Nelson CE, Anderson P, Gates RD 2017. Correspondence of coral holobiont metabolome with symbiotic bacteria, archaea and Symbiodinium communities. Environ. Microbiol. Rep. 9:310–15
    [Google Scholar]
  111. 111. 
    Pogoreutz C, Rädecker N, Cárdenas A, Gärdes A, Wild C, Voolstra CR. 2018. Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome. Ecol. Evol. 8:2240–52
    [Google Scholar]
  112. 112. 
    Bayer T, Neave MJ, Alsheikh-Hussain A, Aranda M, Yum LK et al. 2013. The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Appl. Environ. Microbiol. 79:4759–62
    [Google Scholar]
  113. 113. 
    Neave MJ, Rachmawati R, Xun L, Michell CT, Bourne DG et al. 2016. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J 11:186–200
    [Google Scholar]
  114. 114. 
    Neave MJ, Apprill A, Ferrier-Pagès C, Voolstra CR. 2016. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl. Microbiol. Biotechnol. 100:8315–24
    [Google Scholar]
  115. 115. 
    Breusing C, Mitchell J, Delaney J, Sylva SP, Seewald JS et al. 2020. Physiological dynamics of chemosynthetic symbionts in hydrothermal vent snails. ISME J. 14:2568–79
    [Google Scholar]
  116. 116. 
    Reveillaud J, Anderson R, Reves-Sohn S, Cavanaugh C, Huber JA. 2018. Metagenomic investigation of vestimentiferan tubeworm endosymbionts from Mid-Cayman Rise reveals new insights into metabolism and diversity. Microbiome 6:19
    [Google Scholar]
  117. 117. 
    Rubin-Blum M, Dubilier N, Kleiner M 2019. Genetic evidence for two carbon fixation pathways (the Calvin-Benson-Bassham cycle and the reverse tricarboxylic acid cycle) in symbiotic and free-living bacteria. mSphere 4:e00394-18
    [Google Scholar]
  118. 118. 
    Ikuta T, Takaki Y, Nagai Y, Shimamura S, Tsuda M et al. 2016. Heterogeneous composition of key metabolic gene clusters in a vent mussel symbiont population. ISME J. 10:990–1001
    [Google Scholar]
  119. 119. 
    Hinzke T, Kleiner M, Meister M, Schlüter R, Hentschker C et al. 2021. Bacterial symbiont subpopulations have different roles in a deep-sea symbiosis. eLife 10:e58371
    [Google Scholar]
  120. 120. 
    Soininen J, McDonald R, Hillebrand H. 2007. The distance decay of similarity in ecological communities. Ecography 30:3–12
    [Google Scholar]
  121. 121. 
    Varliero G, Bienhold C, Schmid F, Boetius A, Molari M. 2019. Microbial diversity and connectivity in deep-sea sediments of the South Atlantic Polar Front. Front. Microbiol. 10:665
    [Google Scholar]
  122. 122. 
    Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH. 2012. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10:497–506
    [Google Scholar]
  123. 123. 
    Zhou J, Ning D. 2017. Stochastic community assembly: Does it matter in microbial ecology? Microbiol. . Mol. Biol. Rev. 81:e00002-17
    [Google Scholar]
  124. 124. 
    Easson CG, Lopez JV. 2019. Depth-dependent environmental drivers of microbial plankton community structure in the northern gulf of Mexico. Front. Microbiol. 9:3175
    [Google Scholar]
  125. 125. 
    Kirkpatrick JB, Walsh EA, D'Hondt S. 2019. Microbial selection and survival in subseafloor sediment. Front. Microbiol. 10:956
    [Google Scholar]
  126. 126. 
    Bienhold C, Zinger L, Boetius A, Ramette A. 2016. Diversity and biogeography of bathyal and abyssal seafloor bacteria. PLOS ONE 11:e0148016
    [Google Scholar]
  127. 127. 
    D'Hondt S, Inagaki F, Alvarez Zarikian C, Abrams LJ, Dubois N et al. 2015. Presence of oxygen and aerobic communities from sea floor to basement in deep-sea sediments. Nat. Geosci. 8:299–304
    [Google Scholar]
  128. 128. 
    Baas-Becking LGM. 1934. Geobiologie of Inleiding tot de Milieukunde The Hague, Neth.: van Stockum and Zoon
  129. 129. 
    Ruff SE, Biddle JF, Teske AP, Knittel K, Boetius A et al. 2015. Global dispersion and local diversification of the methane seep microbiome. PNAS 112:4015–20
    [Google Scholar]
  130. 130. 
    Joye SB. 2020. The geology and biogeochemistry of hydrocarbon seeps. Annu. Rev. Earth Planet. Sci. 48:205–31
    [Google Scholar]
  131. 131. 
    Djurhuus A, Mikalsen SO, Giebel HA, Rogers AD. 2017. Cutting through the smoke: the diversity of microorganisms in deep-sea hydrothermal plumes. R. Soc. Open Sci. 4:160829
    [Google Scholar]
  132. 132. 
    Dick GJ. 2019. The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally. Nat. Rev. Microbiol. 17:271–83
    [Google Scholar]
  133. 133. 
    Gonnella G, Böhnke S, Indenbirken D, Garbe-Schönberg D, Seifert R et al. 2016. Endemic hydrothermal vent species identified in the open ocean seed bank. Nat. Microbiol. 1:16086
    [Google Scholar]
  134. 134. 
    Djurhuus A, Boersch-Supan PH, Mikalsen S-O, Rogers AD, et al. 2017. Microbe biogeography tracks water masses in a dynamic oceanic frontal system. R. Soc. Open Sci. 4:3170033
    [Google Scholar]
  135. 135. 
    Ofiţeru ID, Lunn M, Curtis T, Wells GF, Criddle CS et al. 2010. Combined niche and neutral effects in a microbial wastewater treatment community. PNAS 107:3515345–50
    [Google Scholar]
  136. 136. 
    Zhou J, Liu W, Deng Y, Jiang Y-H, Xue K et al. 2013. Stochastic assembly leads to alternative communities with distinct functions in a bioreactor microbial community. mBio 4:e00584-12
    [Google Scholar]
  137. 137. 
    Hubbell SP. 2001. The Unified Neutral Theory of Biodiversity and Biogeography Princeton, NJ: Princeton Univ. Press
  138. 138. 
    Anderson RE, Reveillaud J, Reddington E, Delmont TO, Murat Eren A et al. 2017. Genomic variation in microbial populations inhabiting the marine subseafloor at deep-sea hydrothermal vents. Nat. Commun. 8:1114
    [Google Scholar]
  139. 139. 
    Mende DR, Bryant JA, Aylward FO, Eppley JM, Nielsen T et al. 2017. Environmental drivers of a microbial genomic transition zone in the ocean's interior. Nat. Microbiol. 2:1367–73
    [Google Scholar]
  140. 140. 
    Ücker M, Ansorge R, Sato Y, Sayavedra L, Breusing C. 2021. Deep-sea mussels from a hybrid zone on the Mid-Atlantic Ridge host genetically indistinguishable symbionts. ISME J. 15:3076–83
    [Google Scholar]
  141. 141. 
    DeChaine EG, Bates AE, Shank TM, Cavanaugh CM. 2006. Off-axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal vents. Environ. Microbiol. 8:1902–12
    [Google Scholar]
  142. 142. 
    Brzechffa C, Goffredi SK. 2021. Contrasting influences on bacterial symbiont specificity by co-occurring deep-sea mussels and tubeworms. Environ. Microbiol. Rep. 13:104–11
    [Google Scholar]
  143. 143. 
    Rossbach S, Cardenas A, Perna G, Duarte CM, Voolstra CR. 2019. Tissue-specific microbiomes of the Red Sea giant clam Tridacna maxima highlight differential abundance of Endozoicomonadaceae. Front. Microbiol. 10:2661
    [Google Scholar]
  144. 144. 
    Allali I, Delgado S, Marron PI, Astudillo A, Yeh JJ et al. 2015. Gut microbiome compositional and functional differences between tumor and non-tumor adjacent tissues from cohorts from the US and Spain. Gut Microbes 6:161–72
    [Google Scholar]
  145. 145. 
    Rau GH. 1981. Hydrothermal vent clam and tube worm 13C/12C: further evidence of nonphotosynthetic food sources. Science 213:338–40
    [Google Scholar]
  146. 146. 
    Hahn CJ, Laso-Pérez R, Vulcano F, Vaziourakis K-M, Stokke R et al. 2020.. “ Candidatus Ethanoperedens,” a thermophilic genus of archaea mediating the anaerobic oxidation of ethane. mBio 11:e00600-20
    [Google Scholar]
  147. 147. 
    Kellogg CA, Lisle JT, Galkiewicz JP. 2009. Culture-independent characterization of bacterial communities associated with the cold-water coral Lophelia pertusa in the northeastern Gulf of Mexico. Appl. Environ. Microbiol. 75:2294–303
    [Google Scholar]
  148. 148. 
    Neulinger SC, Järnegren J, Ludvigsen M, Lochte K, Dullo WC 2008. Phenotype-specific bacterial communities in the cold-water coral Lophelia pertusa (Scleractinia) and their implications for the coral's nutrition, health, and distribution. Appl. Environ. Microbiol. 74:7272–85
    [Google Scholar]
  149. 149. 
    Childress JJ, Girguis PR. 2011. The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities. J. Exp. Biol. 214:312–25
    [Google Scholar]
  150. 150. 
    Jan C, Petersen JM, Werner J, Teeling H, Huang S et al. 2014. The gill chamber epibiosis of deep-sea shrimp Rimicaris exoculata: an in-depth metagenomic investigation and discovery of Zetaproteobacteria. Environ. Microbiol. 16:2723–38
    [Google Scholar]
  151. 151. 
    Jiang L, Liu X, Dong C, Huang Z, Cambon-Bonavita M-A et al. 2020.. “ Candidatus desulfobulbus rimicarensis,” an uncultivated deltaproteobacterial epibiont from the deep-sea hydrothermal vent shrimp Rimicaris exoculata. Appl. Environ. Microbiol. 86:e02549-19
    [Google Scholar]
  152. 152. 
    Zbinden M, Cambon-Bonavita M-A. 2020. Rimicaris exoculata: biology and ecology of a shrimp from deep-sea hydrothermal vents associated with ectosymbiotic bacteria. Mar. Ecol. Prog. Ser. 652:187–222
    [Google Scholar]
  153. 153. 
    Levin LA, Bett BJ, Gates AR, Heimbach P, Howe BM et al. 2019. Global observing needs in the deep ocean. Front. Mar. Sci. 6:241
    [Google Scholar]
  154. 154. 
    Pratte ZA, Kellogg CA. 2021. Comparison of preservation and extraction methods on five taxonomically disparate coral microbiomes. Front. Mar. Sci. 8:938
    [Google Scholar]
  155. 155. 
    Geier B, Sogin EM, Michellod D, Janda M, Kompauer M et al. 2020. Spatial metabolomics of in situ host–microbe interactions at the micrometre scale. Nat. Microbiol. 5:498–510
    [Google Scholar]
  156. 156. 
    Orcutt BN, Sylvan JB, Knab NJ, Edwards KJ. 2011. Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol. Mol. Biol. Rev. 75:361–422
    [Google Scholar]
  157. 157. 
    Sievert SM, Vetriani C. 2012. Chemoautotrophy at deep-sea vents: past, present, and future. Oceanography 25:218–33
    [Google Scholar]
  158. 158. 
    Dando PR, Southward AF, Southward EC, Dixon DR, Crawford A, Crawford M. 1992. Shipwrecked tube worms. Nature 356:667
    [Google Scholar]
  159. 159. 
    Hughes DJ, Crawford M. 2008. A new record of the vestimentiferan Lamellibrachia sp. (Polychaeta: Siboglinidae) from a deep shipwreck in the eastern Mediterranean. Mar. Biodivers. Rec. 1:e21
    [Google Scholar]
  160. 160. 
    Gambi MC, Schulze A, Amato E. 2011. Record of Lamellibrachia sp. (Annelida: Siboglinidae: Vestimentifera) from a deep shipwreck in the western Mediterranean Sea (Italy). Mar. Biodivers. Rec. 4:e24
    [Google Scholar]
/content/journals/10.1146/annurev-animal-081621-112021
Loading
/content/journals/10.1146/annurev-animal-081621-112021
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error