1932

Abstract

Possibly the last discovery of a previously unknown major ecosystem on Earth was made just over half a century ago, when researchers found teaming communities of animals flourishing two and a half kilometers below the ocean surface at hydrothermal vents. We now know that these highly productive ecosystems are based on nutritional symbioses between chemosynthetic bacteria and eukaryotes and that these chemosymbioses are ubiquitous in both deep-sea and shallow-water environments. The symbionts are primary producers that gain energy from the oxidation of reduced compounds, such as sulfide and methane, to fix carbon dioxide or methane into biomass to feed their hosts. This review outlines how the symbiotic partners have adapted to living together. We first focus on the phylogenetic and metabolic diversity of these symbioses and then highlight selected research directions that could advance our understanding of the processes that shaped the evolutionary and ecological success of these associations.

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2021-10-08
2024-06-14
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Literature Cited

  1. 1. 
    Altamia MA, Shipway JR, Concepcion GP, Haygood MG, Distel DL. 2019. Thiosocius teredinicola gen. nov., sp. nov., a sulfur-oxidizing chemolithoautotrophic endosymbiont cultivated from the gills of the giant shipworm, Kuphus polythalamius. Int. J. Syst. Evol. Microbiol. 69:638–44
    [Google Scholar]
  2. 2. 
    Ansorge R, Romano S, Sayavedra L, Porras MÁG, Kupczok A et al. 2019. Functional diversity enables multiple symbiont strains to coexist in deep-sea mussels. Nat. Microbiol. 4:2487–97
    [Google Scholar]
  3. 3. 
    Assié A, Leisch N, Meier DV, Gruber-Vodicka H, Tegetmeyer HE et al. 2020. Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria). ISME J 14:104–22
    [Google Scholar]
  4. 4. 
    Bates AE, Harmer TL, Roeselers G, Cavanaugh CM. 2011. Phylogenetic characterization of episymbiotic bacteria hosted by a hydrothermal vent limpet (Lepetodrilidae, Vetigastropoda). Biol. Bull. 220:118–27
    [Google Scholar]
  5. 5. 
    Beinart RA. 2019. The significance of microbial symbionts in ecosystem processes. mSystems 4:e00127-19
    [Google Scholar]
  6. 6. 
    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. 27:1794–807
    [Google Scholar]
  7. 7. 
    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]
  8. 8. 
    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
    [Google Scholar]
  9. 9. 
    Bergin C, Wentrup C, Brewig N, Blazejak A, Erséus 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]
  10. 10. 
    Borowski C, Giere O, Krieger J, Amann R, Dubilier N. 2002. New aspects of the symbiosis in the provannid snail Ifremeria nautilei from the North Fiji Back Arc Basin. Cahiers Biol. Mar. 43:321–24
    [Google Scholar]
  11. 11. 
    Breusing C, Schultz DT, Sudek S, Worden AZ, Young CR. 2020. High-contiguity genome assembly of the chemosynthetic gammaproteobacterial endosymbiont of the cold seep tubeworm Lamellibrachia barhami. Mol. Ecol. Resour. 20:1432–44
    [Google Scholar]
  12. 12. 
    Bright M, Keckeis H, Fisher C. 2000. An autoradiographic examination of carbon fixation, transfer and utilization in the Riftia pachyptila symbiosis. Mar. Biol. 136:621–32
    [Google Scholar]
  13. 13. 
    Bright M, Sorgo A. 2003. Ultrastructural reinvestigation of the trophosome in adults of Riftia pachyptila (Annelida, Siboglinidae). Invertebrate Biol 122:347–68
    [Google Scholar]
  14. 14. 
    Campbell BJ, Stein JL, Cary SC. 2003. Evidence of chemolithoautotrophy in the bacterial community associated with Alvinella pompejana, a hydrothermal vent polychaete. Appl. Environ. Microbiol. 69:5070–78
    [Google Scholar]
  15. 15. 
    Cary SC, Fisher CR, Felbeck H. 1988. Mussel growth supported by methane as sole carbon and energy source. Science 240:78–80
    [Google Scholar]
  16. 16. 
    Cavanaugh CM, Levering PR, Maki JS, Mitchell R, Lidstrom ME. 1987. Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature 325:346–48
    [Google Scholar]
  17. 17. 
    Cavanaugh CM, McKiness Z, Newton IL, Stewart FJ 2006. Marine chemosynthetic symbioses. Prokaryotes 1:475–507
    [Google Scholar]
  18. 18. 
    Cavanaugh CM, Robinson JJ. 1996. CO2 fixation in chemoautotroph-invertebrate symbioses: expression of form I and form II RuBisCO. Microbial Growth on C1 Compounds ME Lidstrom, FR Tabita 285–92 Dordrecht, Neth: Springer
    [Google Scholar]
  19. 19. 
    Cecil JD, Sirisaengtaksin N, O'Brien-Simpson NM, Krachler AM. 2019. Outer membrane vesicle-host cell interactions. Microbiol. Spectr 7: https://doi.org/10.1128/microbiolspec.PSIB-0001-2018
    [Crossref] [Google Scholar]
  20. 20. 
    Childress JJ, Fisher C, Brooks J, Kennicutt M, Bidigare R, Anderson A 1986. A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas. Science 233:1306–8
    [Google Scholar]
  21. 21. 
    Childress JJ, Girguis PR. 2011. The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities. J. Exp. Biol. 214:312
    [Google Scholar]
  22. 22. 
    Coale KH, Chin CS, Massoth GJ, Johnson KS, Baker ET. 1991. In situ chemical mapping of dissolved iron and manganese in hydrothermal plumes. Nature 352:325–28
    [Google Scholar]
  23. 23. 
    Colaço A, Bettencourt R, Costa V, Lino S, Lopes H et al. 2011. LabHorta: a controlled aquarium system for monitoring physiological characteristics of the hydrothermal vent mussel Bathymodiolus azoricus. ICES J. Mar. Sci. 68:349–56
    [Google Scholar]
  24. 24. 
    Crowther GJ, Kosály G, Lidstrom ME. 2008. Formate as the main branch point for methylotrophic metabolism in Methylobacterium extorquens AM1. J. Bacteriol. 190:5057
    [Google Scholar]
  25. 25. 
    Cunning R, Muller EB, Gates RD, Nisbet RM. 2017. A dynamic bioenergetic model for coral-Symbiodinium symbioses and coral bleaching as an alternate stable state. J. Theor. Biol. 431:49–62
    [Google Scholar]
  26. 26. 
    Dattagupta S, Schaperdoth I, Montanari A, Mariani S, Kita N et al. 2009. A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod. ISME J 3:935–43
    [Google Scholar]
  27. 27. 
    Dick GJ. 2019. The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally. Nat. Rev. Microbiol. 17:271–83
    [Google Scholar]
  28. 28. 
    Distel DL, Felbeck H, Cavanaugh CM. 1994. Evidence for phylogenetic congruence among sulfur-oxidizing chemoautotrophic bacterial endosymbionts and their bivalve hosts. J. Mol. Evol. 38:533–42
    [Google Scholar]
  29. 29. 
    Distel DL, Lane DJ, Olsen GJ, Giovannoni SJ, Pace B et al. 1988. Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences. J. Bacteriol. 170:2506
    [Google Scholar]
  30. 30. 
    Dmytrenko O, Russell SL, Loo WT, Fontanez KM, Liao L et al. 2014. The genome of the intracellular bacterium of the coastal bivalve, Solemya velum: a blueprint for thriving in and out of symbiosis. BMC Genom 15:1–20
    [Google Scholar]
  31. 31. 
    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]
  32. 32. 
    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]
  33. 33. 
    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]
  34. 34. 
    Durand L, Zbinden M, Cueff-Gauchard V, Duperron S, Roussel EG et al. 2009. Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community. FEMS Microbiol. Ecol. 71:291–303
    [Google Scholar]
  35. 35. 
    Durand P, Gros O. 1996. Bacterial host specificity of Lucinacea endosymbionts: interspecific variation in 16S rRNA sequences. FEMS Microbiol. Lett. 140:193–98
    [Google Scholar]
  36. 36. 
    Edgcomb VP, Breglia SA, Yubuki N, Beaudoin D, Patterson DJ et al. 2011. Identity of epibiotic bacteria on symbiontid euglenozoans in O2-depleted marine sediments: evidence for symbiont and host co-evolution. ISME J 5:231–43
    [Google Scholar]
  37. 37. 
    Eichinger I, Schmitz-Esser S, Schmid M, Fisher CR, Bright M. 2014. Symbiont-driven sulfur crystal formation in a thiotrophic symbiosis from deep-sea hydrocarbon seeps. Environ. Microbiol. Rep. 6:364–72
    [Google Scholar]
  38. 38. 
    Engelberts JP, Robbins SJ, de Goeij JM, Aranda M, Bell SC, Webster NS. 2020. Characterization of a sponge microbiome using an integrative genome-centric approach. ISME J 14:1100–10
    [Google Scholar]
  39. 39. 
    Feely RA, Trefry JH, Lebon GT, German CR. 1998. The relationship between P/Fe and V/Fe ratios in hydrothermal precipitates and dissolved phosphate in seawater. Geophys. Res. Lett. 25:2253–56
    [Google Scholar]
  40. 40. 
    Fisher C, Childress J, Sanders N. 1988. The role of vestimentiferan hemoglobin in providing an environment suitable for chemoautotrophic sulfide-oxidizing endosymbionts. Symbiosis 5:229–46
    [Google Scholar]
  41. 41. 
    Flot J-F, Bauermeister J, Brad T, Hillebrand-Voiculescu A, Sarbu SM, Dattagupta S. 2014. NiphargusThiothrix associations may be widespread in sulphidic groundwater ecosystems: evidence from southeastern Romania. Mol. Ecol. 23:1405–17
    [Google Scholar]
  42. 42. 
    Forget NL, Perez M, Juniper SK. 2015. Molecular study of bacterial diversity within the trophosome of the vestimentiferan tubeworm Ridgeia piscesae. Mar. Ecol. 36:35–44
    [Google Scholar]
  43. 43. 
    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]
  44. 44. 
    Geier B. 2018. Micro CT of Bathymodiolus azoricus. Figshare https://doi.org/10.6084/m9.figshare.5458234.v1
    [Crossref] [Google Scholar]
  45. 45. 
    Giere O, Conway N, Gastrock G, Schmidt C. 1991. 'Regulation' of gutless annelid ecology by endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 68:287–99
    [Google Scholar]
  46. 46. 
    Girguis PR, Lee RW, Desaulniers N, Childress JJ, Pospesel M et al. 2000. Fate of nitrate acquired by the tubeworm Riftia pachyptila. Appl. Environ. Microbiol. 66:2783
    [Google Scholar]
  47. 47. 
    Goffredi SK, Jones WJ, Erhlich H, Springer A, Vrijenhoek RC. 2008. Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta. Environ. Microbiol. 10:2623–34
    [Google Scholar]
  48. 48. 
    Goffredi SK, Tilic E, Mullin SW, Dawson KS, Keller A et al. 2020. Methanotrophic bacterial symbionts fuel dense populations of deep-sea feather duster worms (Sabellida, Annelida) and extend the spatial influence of methane seepage. Sci. Adv. 6:eaay8562
    [Google Scholar]
  49. 49. 
    Gruber-Vodicka HR, Dirks U, Leisch N, Baranyi C, Stoecker K et al. 2011. Paracatenula, an ancient symbiosis between thiotrophic Alphaproteobacteria and catenulid flatworms. PNAS 108:12078
    [Google Scholar]
  50. 50. 
    Guezi H, Boutet I, Andersen AC, Lallier F, Tanguy A. 2014. Comparative analysis of symbiont ratios and gene expression in natural populations of two Bathymodiolus mussel species. Symbiosis 63:19–29
    [Google Scholar]
  51. 51. 
    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]
  52. 52. 
    Hambleton EA, Jones VAS, Maegele I, Kvaskoff D, Sachsenheimer T, Guse A 2019. Sterol transfer by atypical cholesterol-binding NPC2 proteins in coral-algal symbiosis. eLife 8:e43923
    [Google Scholar]
  53. 53. 
    Hentschel U, Hand S, Felbeck H. 1996. The contribution of nitrate respiration to the energy budget of the symbiont-containing clam Lucinoma aequizonata: a calorimetric study. J. Exp. Biol. 199:427–33
    [Google Scholar]
  54. 54. 
    Hestetun JT, Dahle H, Jørgensen SL, Olsen BR, Rapp HT. 2016. The microbiome and occurrence of methanotrophy in carnivorous sponges. Front. Microbiol. 7:1781
    [Google Scholar]
  55. 55. 
    Hinzke T, Kleiner M, Breusing C, Felbeck H, Häsler R et al. 2019. Host-microbe interactions in the chemosynthetic Riftia pachyptila symbiosis. mBio 10:e02243-19
    [Google Scholar]
  56. 56. 
    Hügler M, Sievert SM. 2011. Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Annu. Rev. Mar. Sci. 3:261–89
    [Google Scholar]
  57. 57. 
    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]
  58. 58. 
    Imhoff JF, Sahling H, Süling J, Kath T 2003. 16S rDNA-based phylogeny of sulphur-oxidising bacterial endosymbionts in marine bivalves from cold-seep habitats. Mar. Ecol. Prog. Ser. 249:39–51
    [Google Scholar]
  59. 59. 
    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]
  60. 60. 
    Jäckle O, Seah BKB, Tietjen M, Leisch N, Liebeke M et al. 2019. Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm Paracatenula. PNAS 116:8505
    [Google Scholar]
  61. 61. 
    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]
  62. 62. 
    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]
  63. 63. 
    Kleiner M, Petersen JM, Dubilier N. 2012. Convergent and divergent evolution of metabolism in sulfur-oxidizing symbionts and the role of horizontal gene transfer. Curr. Opin. Microbiol. 15:621–31
    [Google Scholar]
  64. 64. 
    Kleiner M, Wentrup C, Holler T, Lavik G, Harder J et al. 2015. Use of carbon monoxide and hydrogen by a bacteria–animal symbiosis from seagrass sediments. Environ. Microbiol. 17:5023–35
    [Google Scholar]
  65. 65. 
    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
    [Google Scholar]
  66. 66. 
    König S, Gros O, Heiden SE, Hinzke T, Thürmer A et al. 2016. Nitrogen fixation in a chemoautotrophic lucinid symbiosis. Nat. Microbiol. 2:16193
    [Google Scholar]
  67. 67. 
    König S, Le Guyader H, Gros O 2015. Thioautotrophic bacterial endosymbionts are degraded by enzymatic digestion during starvation: case study of two lucinids Codakia orbicularis and C. orbiculata. Microsc. Res. Tech. 78:173–79
    [Google Scholar]
  68. 68. 
    Kresge N, Simoni RD, Hill RL. 2005. The discovery of heterotrophic carbon dioxide fixation by Harland G. Wood. J. Biol. Chem. 280:155–57
    [Google Scholar]
  69. 69. 
    Kuwahara H, Yoshida T, Takaki Y, Shimamura S, Nishi S et al. 2007. Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr. Biol. 17:881–86
    [Google Scholar]
  70. 70. 
    Lee R, Childress J. 1994. Assimilation of inorganic nitrogen by marine invertebrates and their chemoautotrophic and methanotrophic symbionts. Appl. Environ. Microbiol. 60:1852–58
    [Google Scholar]
  71. 71. 
    Lee RW, Childress JJ. 1996. Inorganic N assimilation and ammonium pools in a deep-sea mussel containing methanotrophic endosymbionts. Biol. Bull. 190:373–84
    [Google Scholar]
  72. 72. 
    Lee RW, Robinson JJ, Cavanaugh CM. 1999. Pathways of inorganic nitrogen assimilation in chemoautotrophic bacteria-marine invertebrate symbioses: expression of host and symbiont glutamine synthetase. J. Exp. Biol. 202:289
    [Google Scholar]
  73. 73. 
    Li Y, Liles MR, Halanych KM. 2018. Endosymbiont genomes yield clues of tubeworm success. ISME J 12:2785–95
    [Google Scholar]
  74. 74. 
    Lim SJ, Davis BG, Gill DE, Walton J, Nachman E et al. 2019. Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species. ISME J 13:902–20
    [Google Scholar]
  75. 75. 
    Liu M, Fan L, Zhong L, Kjelleberg S, Thomas T. 2012. Metaproteogenomic analysis of a community of sponge symbionts. ISME J 6:1515–25
    [Google Scholar]
  76. 76. 
    Markert S, Arndt C, Felbeck H, Becher D, Sievert SM et al. 2007. Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science 315:247–50
    [Google Scholar]
  77. 77. 
    Martins I, Colaço A, Dando PR, Martins I, Desbruyeres D et al. 2008. Size-dependent variations on the nutritional pathway of Bathymodiolus azoricus demonstrated by a C-flux model. Ecol. Modell. 217:59–71
    [Google Scholar]
  78. 78. 
    McCuaig B, Peña-Castillo L, Dufour SC. 2020. Metagenomic analysis suggests broad metabolic potential in extracellular symbionts of the bivalve Thyasira cf. gouldi. Anim. Microbiome 2:7
    [Google Scholar]
  79. 79. 
    Meier DV, Pjevac P, Bach W, Hourdez S, Girguis PR et al. 2017. Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents. ISME J 11:1545–58
    [Google Scholar]
  80. 80. 
    Mitchell JH, Leonard JM, Delaney J, Girguis PR, Scott KM. 2019. Hydrogen does not appear to be a major electron donor for symbiosis with the deep-sea hydrothermal vent tubeworm Riftia pachyptila. Appl. Environ. Microbiol. 86:e01522-19
    [Google Scholar]
  81. 81. 
    Miyazaki J, Ikuta T, Watsuji TO, Abe M, Yamamoto M et al. 2020. Dual energy metabolism of the Campylobacterota endosymbiont in the chemosynthetic snail Alviniconcha marisindica. ISME J 14:1273–89
    [Google Scholar]
  82. 82. 
    Mohamed NM, Saito K, Tal Y, Hill RT. 2010. Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J 4:38–48
    [Google Scholar]
  83. 83. 
    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. 9:1345–53
    [Google Scholar]
  84. 84. 
    Muscatine L, Porter JW. 1977. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–60
    [Google Scholar]
  85. 85. 
    Nakagawa S, Shimamura S, Takaki Y, Suzuki Y, Murakami S et al. 2014. Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont. ISME J 8:40–51
    [Google Scholar]
  86. 86. 
    Nelson DC, Fisher CR. 1995. Chemoautotrophic and methanotrophic endosymbiotic bacteria at deep-sea vents and seeps. Microbiology of Deep-Sea Hydrothermal Vents DM Karl 125–67 Boca Raton, FL: CRC
    [Google Scholar]
  87. 87. 
    Nelson K, Fisher CR. 2000. Absence of cospeciation in deep-sea vestimentiferan tube worms and their bacterial endosymbionts. Symbiosis 28:1–15
    [Google Scholar]
  88. 88. 
    Newton ILG, Woyke T, Auchtung TA, Dilly GF, Dutton RJ et al. 2007. The Calyptogena magnifica, chemoautotrophic symbiont genome. Science 315:998–1000
    [Google Scholar]
  89. 89. 
    Nix ER, Fisher CR, Vodenichar J, Scott KM. 1995. Physiological ecology of a mussel with methanotrophic endosymbionts at three hydrocarbon seep sites in the Gulf of Mexico. Mar. Biol. 122:605–17
    [Google Scholar]
  90. 90. 
    Pasulka AL, Goffredi SK, Tavormina PL, Dawson KS, Levin LA et al. 2017. Colonial tube-dwelling ciliates influence methane cycling and microbial diversity within methane seep ecosystems. Front. Mar. Sci. 3:276
    [Google Scholar]
  91. 91. 
    Peek AS, Feldman RA, Lutz RA, Vrijenhoek RC 1998. Cospeciation of chemoautotrophic bacteria and deep sea clams. PNAS 95:9962
    [Google Scholar]
  92. 92. 
    Pende N, Wang J, Weber PM, Verheul J, Kuru E et al. 2018. Host-polarized cell growth in animal symbionts. Curr. Biol. 28:1039–51.e5
    [Google Scholar]
  93. 93. 
    Perez RC, Matin A. 1982. Carbon dioxide assimilation by Thiobacillus novellus under nutrient-limited mixotrophic conditions. J. Bacteriol. 150:46–51
    [Google Scholar]
  94. 94. 
    Petersen JM, Kemper A, Gruber-Vodicka H, Cardini U, van der Geest M et al. 2016. Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation. Nat. Microbiol. 2:16195 Erratum. 2018. Nat. Microbiol. 3:961
    [Google Scholar]
  95. 95. 
    Petersen JM, Ramette A, Lott C, Cambon-Bonavita M-A, Zbinden M, Dubilier N. 2010. Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma- and epsilonproteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields. Environ. Microbiol. 12:2204–18
    [Google Scholar]
  96. 96. 
    Petersen JM, Zielinski FU, Pape T, Seifert R, Moraru C et al. 2011. Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476:176–80
    [Google Scholar]
  97. 97. 
    Ponnudurai R, Kleiner M, Sayavedra L, Petersen JM, Moche M et al. 2017. Metabolic and physiological interdependencies in the Bathymodiolus azoricus symbiosis. ISME J 11:463–77
    [Google Scholar]
  98. 98. 
    Ponsard J, Cambon-Bonavita M-A, Zbinden M, Lepoint G, Joassin A et al. 2013. Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata. ISME J 7:96–109
    [Google Scholar]
  99. 99. 
    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 6:1–15
    [Google Scholar]
  100. 100. 
    Rinke C, Schmitz-Esser S, Loy A, Horn M, Wagner M, Bright M. 2009. High genetic similarity between two geographically distinct strains of the sulfur-oxidizing symbiont ‘Candidatus Thiobios zoothamnicoli’. FEMS Microbiol. Ecol. 67:229–41
    [Google Scholar]
  101. 101. 
    Riou V, Halary S, Duperron S, Bouillon S, Elskens M et al. 2008. Influence of CH4 and H2 availability on symbiont distribution, carbon assimilation and transfer in the dual symbiotic vent mussel Bathymodiolus azoricus. Biogeosciences 5:1681–91
    [Google Scholar]
  102. 102. 
    Robidart JC, Bench SR, Feldman RA, Novoradovsky A, Podell SB et al. 2008. Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ. Microbiol. 10:727–37
    [Google Scholar]
  103. 103. 
    Rodrigues CF, Hilário A, Cunha MR, Weightman AJ, Webster G. 2011. Microbial diversity in Frenulata (Siboglinidae, Polychaeta) species from mud volcanoes in the Gulf of Cadiz (NE Atlantic). Antonie van Leeuwenhoek 100:83–98
    [Google Scholar]
  104. 104. 
    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]
  105. 105. 
    Roslev P, Larsen MB, Jørgensen D, Hesselsoe M. 2004. Use of heterotrophic CO2 assimilation as a measure of metabolic activity in planktonic and sessile bacteria. J. Microbiol. Methods 59:381–93
    [Google Scholar]
  106. 106. 
    Rubin-Blum M, Antony CP, Sayavedra L, Martínez-Pérez C, Birgel D et al. 2019. Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts. ISME J 13:1209–25
    [Google Scholar]
  107. 107. 
    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]
  108. 108. 
    Ruehland C, Dubilier N. 2010. Gamma- and epsilonproteobacterial ectosymbionts of a shallow-water marine worm are related to deep-sea hydrothermal vent ectosymbionts. Environ. Microbiol. 12:2312–26
    [Google Scholar]
  109. 109. 
    Ruff SE, Biddle JF, Teske AP, Knittel K, Boetius A, Ramette A 2015. Global dispersion and local diversification of the methane seep microbiome. PNAS 112:4015
    [Google Scholar]
  110. 110. 
    Sánchez-Andrea I, Guedes IA, Hornung B, Boeren S, Lawson CE et al. 2020. The reductive glycine pathway allows autotrophic growth of Desulfovibrio desulfuricans. Nat. Commun. 11:1–12
    [Google Scholar]
  111. 111. 
    Sanders JG, Beinart RA, Stewart FJ, Delong EF, Girguis PR. 2013. Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. ISME J 7:1556–67
    [Google Scholar]
  112. 112. 
    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]
  113. 113. 
    Schimak MP, Toenshoff ER, Bright M. 2012. Simultaneous 16S and 18S rRNA fluorescence in situ hybridization (FISH) on LR White sections demonstrated in Vestimentifera (Siboglinidae) tubeworms. Acta Histochem 114:122–30
    [Google Scholar]
  114. 114. 
    Schönheit P, Buckel W, Martin WF. 2016. On the origin of heterotrophy. Trends Microbiol 24:12–25
    [Google Scholar]
  115. 115. 
    Schwechheimer C, Kuehn MJ. 2015. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat. Rev. Microbiol. 13:605–19
    [Google Scholar]
  116. 116. 
    Scott KM, Fisher CR. 1995. Physiological ecology of sulfide metabolism in hydrothermal vent and cold seep Vesicomyid clams and Vestimentiferan tubeworms. Am. Zool. 35:102–11
    [Google Scholar]
  117. 117. 
    Seah BK, Schwaha T, Volland J-M, Huettel B, Dubilier N, Gruber-Vodicka HR 2017. Specificity in diversity: single origin of a widespread ciliate-bacteria symbiosis. Proc. R. Soc. B 284:20170764
    [Google Scholar]
  118. 118. 
    Seah BK, Volland J-M, Leisch N, Schwaha T, Dubilier N, Gruber-Vodicka HR. 2020. Kentrophoros magnus sp. nov. (Ciliophora, Karyorelictea), a new flagship species of marine interstitial ciliates. bioRxiv https://doi.org/10.1101/2020.03.19.998534
    [Crossref] [Google Scholar]
  119. 119. 
    Seah BKB, Antony CP, Huettel B, Zarzycki J, Schada von Borzyskowski L et al. 2019. Sulfur-oxidizing symbionts without canonical genes for autotrophic CO2 fixation. mBio 10:e01112-19
    [Google Scholar]
  120. 120. 
    Suzuki Y, Kojima S, Sasaki T, Suzuki M, Utsumi T et al. 2006. Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Appl. Environ. Microbiol. 72:1388–93
    [Google Scholar]
  121. 121. 
    Suzuki Y, Suzuki M, Tsuchida S, Takai K, Horikoshi K et al. 2009. Molecular investigations of the stalked barnacle Vulcanolepas osheai and the epibiotic bacteria from the Brothers Caldera, Kermadec Arc, New Zealand. J. Mar. Biol. Assoc. U.K. 89:727–33
    [Google Scholar]
  122. 122. 
    Thingstad TF. 2000. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45:1320–28
    [Google Scholar]
  123. 123. 
    Thornhill DJ, Wiley AA, Campbell AL, Bartol FF, Teske A, Halanych KM. 2008. Endosymbionts of Siboglinum fiordicum and the phylogeny of bacterial endosymbionts in Siboglinidae (Annelida). Biol. Bull. 214:135–44
    [Google Scholar]
  124. 124. 
    Tian R-M, Zhang W, Cai L, Wong Y-H, Ding W, Qian P-Y. 2017. Genome reduction and microbe-host interactions drive adaptation of a sulfur-oxidizing bacterium associated with a cold seep sponge. mSystems 2:e00184-16
    [Google Scholar]
  125. 125. 
    van Dover CL. 2000. The Ecology of Deep-Sea Hydrothermal Vents Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  126. 126. 
    van Hoek AHAM, van Alen TA, Sprakel VSI, Leunissen JAM, Brigge T et al. 2000. Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol. Biol. Evol. 17:251–58
    [Google Scholar]
  127. 127. 
    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 2020.02.27.968453. https://doi.org/10.1101/2020.02.27.968453
    [Crossref]
  128. 128. 
    Watsuji T, Nakagawa S, Tsuchida S, Toki T, Hirota A et al. 2010. Diversity and function of epibiotic microbial communities on the galatheid crab. Shinkaia crosnieri. Microbes Environ. 25:288–94
    [Google Scholar]
  129. 129. 
    Watsuji T, Yamamoto A, Takaki Y, Ueda K, Kawagucci S, Takai K 2014. Diversity and methane oxidation of active epibiotic methanotrophs on live Shinkaia crosnieri. ISME J 8:102031
    [Google Scholar]
  130. 130. 
    Winogradsky S. 1887. Ueber Schwefelbacterien. Botanische Zeitung 45:606–10
    [Google Scholar]
  131. 131. 
    Winogradsky S. 1890. Recherches sur les organisms de la nitrification. Ann. Inst. Pasteur 4:213–31
    [Google Scholar]
  132. 132. 
    Won Y-J, Jones WJ, Vrijenhoek RC. 2008. Absence of cospeciation between deep-sea Mytilids and their thiotrophic endosymbionts. J. Shellfish Res. 27:129–38
    [Google Scholar]
  133. 133. 
    Wong YH, Sun J, He LS, Chen LG, Qiu J-W, Qian P-Y. 2015. High-throughput transcriptome sequencing of the cold seep mussel Bathymodiolus platifrons. Sci. Rep. 5:16597
    [Google Scholar]
  134. 134. 
    Woyke T, Teeling H, Ivanova NN, Huntemann M, Richter M et al. 2006. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443:950–55
    [Google Scholar]
  135. 135. 
    Yoshihiro F, Chiaki K, Noriaki M, Katsunori F, Shigeaki K. 2001. Dual symbiosis in the cold-seep thyasirid clam Maorithyas hadalis from the hadal zone in the Japan Trench, western Pacific. Mar. Ecol. Prog. Ser. 214:151–59
    [Google Scholar]
  136. 136. 
    Zbinden M, Marqué L, Gaudron SM, Ravaux J, Léger N, Duperron S. 2015. Epsilonproteobacteria as gill epibionts of the hydrothermal vent gastropod Cyathermia naticoides (North East-Pacific Rise). Mar. Biol. 162:435–48
    [Google Scholar]
  137. 137. 
    Zimmermann J, Lott C, Weber M, Ramette A, Bright M et al. 2014. Dual symbiosis with co-occurring sulfur-oxidizing symbionts in vestimentiferan tubeworms from a Mediterranean hydrothermal vent. Environ. Microbiol. 16:3638–56
    [Google Scholar]
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