Dual energy metabolism of the Campylobacterota endosymbiont in the chemosynthetic snail Alviniconcha marisindica.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
07
06
2019
accepted:
30
01
2020
revised:
16
01
2020
pubmed:
14
2
2020
medline:
30
10
2020
entrez:
14
2
2020
Statut:
ppublish
Résumé
Some deep-sea chemosynthetic invertebrates and their symbiotic bacteria can use molecular hydrogen (H
Identifiants
pubmed: 32051527
doi: 10.1038/s41396-020-0605-7
pii: 10.1038/s41396-020-0605-7
pmc: PMC7174374
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1273-1289Références
Lonsdale PA. A deep-sea hydrothermal site on a strike-slip fault. Nature. 1979;281:531–34.
Jones ML. Riftia pachyptila Jones: observations on the vestimentiferan worm from the Galapagos Rift. Science. 1981;213:333–36.
pubmed: 17819904
Felbeck H. Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimentifera). Science. 1981;213:336–38.
pubmed: 17819905
Rau GH. Hydrothermal vent clam and tube worm
pubmed: 17819906
Cavanaugh CL, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB. Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science. 1981;213:340–42.
pubmed: 17819907
Dubilier N, Bergin C, Lott C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol. 2008;6:725–40.
pubmed: 18794911
Campbell BJ, Jeanthon C, Kostka JE, Luther GW III, Cary SC. Growth and phylogenetic properties of novel bacteria belonging to the epsilon subdivision of the Proteobacteria enriched from Alvinella pompejana and deep-sea hydrothermal vents. Appl Environ Microbiol. 2001;67:4566–72.
pubmed: 11571157
pmcid: 93204
Alain K, Querellou J, Lesongeur F, Pignet P, Crassous P, Raguenes G, et al. Cambon-Bonavita MA. Caminibacter hydrogeniphilus gen. nov., sp. nov., a novel thermophilic, hydrogen-oxidizing bacterium isolated from an East Pacific Rise hydrothermal vent. Int J Syst Evol Microbiol. 2002;52:1317–23.
pubmed: 12148646
Miroshnichenko ML, Kostrikina NA, L’Haridon S, Jeanthon C, Hippe H, Stackebrandt E, et al. Nautilia lithotrophica gen. nov., sp. nov., a thermophilic sulfur-reducing ε-proteobacterium isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol. 2002;52:1299–304.
pubmed: 12148643
Takai K, Campbell BJ, Cary SC, Suzuki M, Oida H, Nunoura T, et al. Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Appl Environ Microbiol. 2005;71:7310–20.
pubmed: 16269773
pmcid: 1287660
Takai K, Nakamura K. Compositional, physiological and metabolic variability in microbial communities associated with geochemically diverse, deep-sea hydrothermal vent fluids. In: Barton L, Mendl M, Loy A, editors. Geomicrobiology: molecular & environmental perspective. NY: Springer; 2010. p. 251–83.
Nakamura K, Takai K. Theoretical constraints of physical and chemical properties of hydrothermal fluids on variations in chemolithotrophic microbial communities in seafloor hydrothermal. Prog Earth Planet Sci. 2014. https://doi.org/10.1186/2197-4284-1-5 .
doi: 10.1186/2197-4284-1-5
Petersen JM, Zielinski FU, Pape T, Seifert R, Moraru C, Amann R, et al. Hydrogen is an energy source for hydrothermal vent symbioses. Nature. 2011;476:176–80.
pubmed: 21833083
Beinart RA, Sanders JG, Faure B, Sylva SP, Lee RW, Becker EL, et al. Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses. Proc Natl Acad Sci USA. 2012;109:E3241–50.
pubmed: 23091033
Waite DW, Vanwonterghem I, Rinke C, Parks DH, Zhang Y, et al. Comparative genomic analysis of the class Epsilonproteobacteria and proposed reclassification to Epsilonbacteraeota (phyl. nov.). Front Microbiol. 2017;8:4962–19.
Sanders JG, Beinart RA, Stewart FJ, Delong EF, Girguis PR. Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. ISME J. 2013;7:1556–67.
pubmed: 23619306
pmcid: 3721115
Ikuta T, Takaki Y, Nagai Y, Shimamura S, Tsuda M, Kawagucci S, et al. Heterogeneous composition of key metabolic gene clusters in a vent mussel symbiont population. ISME J. 2016;10:990–1001.
pubmed: 26418631
Markert S, Arndt C, Felbeck H, Becher D, Sievert SM, Hügler M, et al. Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science. 2007;315:247–50.
pubmed: 17218528
Nakagawa S, Shimamura S, Takaki Y, Suzuki Y, Murakami S, Watanabe T, et al. Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont. ISME J. 2014;8:40–51.
pubmed: 23924784
Li Y, Liles MR, Halanych KM. Endosymbiont genomes yield clues of tubeworm success. ISME J. 2018;12:2785–95.
pubmed: 30022157
pmcid: 6194059
Warén A, Bouchet P. Gastropoda and monoplacophora from hydrothermal vents and seeps; new taxa and records. Veliger. 2001;44:116–231.
Suzuki Y, Kojima S, Sasaki T, Suzuki M, Utsumi T, Watanabe H, et al. Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Appl Environ Microbiol. 2006;72:1388–93.
pubmed: 16461691
pmcid: 1392889
Johnson SB, Warén A, Tunnicliffe V, Dover CV, Wheat CG, Schultz TF, et al. Molecular taxonomy and naming of five cryptic species of Alviniconcha snails (Gastropoda: Abyssochrysoidea) from hydrothermal vents. Syst Biodivers. 2014;13:278–95.
Stein JL, Cary SC, Hessler RR, Ohta S, Vetter RD, Childress JJ, et al. Chemoautotrophic symbiosis in a hydrothermal vent gastropod. Biol Bull. 1988;174:373–8.
Suzuki Y, Sasaki T, Suzuki M, Tsuchida S, Nealson KH, Horikoshi K. Molecular phylogenetic and isotopic evidence of two lineages of chemoautotrophic endosymbionts distinct at the subdivision level harbored in one host-animal type: the genus Alviniconcha (Gastropoda: Provannidae). FEMS Microbiol Ecol. 2005;249:105–12.
Suzuki Y, Sasaki T, Suzuki M, Nogi Y, Miwa T, Takai K, et al. Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha marisindica (Gastropoda: Provannidae) from the Indian Ocean. Appl Environ Microbiol. 2005;71:5440–50.
pubmed: 16151136
pmcid: 1214688
Hashimoto J, Ohta S, Gamo T, Chiba H, Yamaguchi T, Tsuchida S, et al. First hydrothermal vent communities from the Indian Ocean discovered. Zool Sci. 2001;18:717–21.
Van Dover CL, Humphris SE, Fornari D, Cavanaugh CM, Collier R, Goffredi SK, et al. Biogeography and ecological setting of Indian Ocean hydrothermal vents. Science. 2001;294:818–23.
pubmed: 11557843
Gallant RM, Von Damm KL. Geochemical controls on hydrothermal fluids from the Kairei and Edmond vent fields, 23°-25°S, Central Indian Ridge. Geochem Geophys Geosyst. 2006;7:Q06018.
Kumagai H, Nakamura K, Toki T, Morishita T, Okino K, Ishibashi J, et al. Geological background of the Kairei and Edmond hydrothermal fields along the Central Indian Ridge: implications of their vent fluids’ distinct chemistry. Geofluid. 2008;8:239–51.
Nakamura K, Morishita T, Bach W, Klein F, Hara K, Okino K, et al. Serpentinized troctolites exposed near the Kairei hydrothermal field, Central Indian Ridge: insights into the origin of the Kairei hydrothermal fluid supporting a unique microbial ecosystem. Earth Planet Sci Lett. 2009;193:371–9.
Miyazaki J, Makabe A, Matsui Y, Ebina N, Tsutsumi S, Ishibashi J, et al. WHATS-3: an improved flow-through multi-bottle fluid sampler for deep-sea geofluid research. Front Earth Sci. 2017;5:202–13.
Takai K, Gamo T, Tsunogai U, Nakayama N, Hirayama H, Nealson KH, et al. Geochemical and microbiological evidence for a hydrogen-based, hyperthermophilic subsurface lithoautotrophic microbial ecosystem (HyperSLiME) beneath an active deep-sea hydrothermal field. Extremophiles. 2004;8:269–82.
pubmed: 15309563
Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K, Horikoshi K. Deep-sea vent ε-proteobacterial genomes provide insights into emergence of pathogens. Proc Natl Acad Sci USA. 2007;104:12146–50.
pubmed: 17615243
Yamamoto M, Nakagawa S, Shimamura S, Takai K, Horikoshi K. Molecular characterization of inorganic sulfur-compound metabolism in the deep-sea epsilonproteobacterium Sulfurovum sp. NBC37-1. Environ Microbiol. 2010;12:1144–53.
pubmed: 20132283
Kawagucci S, Miyazaki J, Noguchi T, Okamura K, Shibuya T, Watsuji T, et al. Fluid chemistry in the Solitaire and Dodo hydrothermal fields of the Central Indian Ridge. Geofluids. 2016;16:988–1005.
Fogo JK, Chemistry MPA. Spectrophotometric determination of hydrogen sulfide. Anal Chem. 1949;21:732–4.
Cline J. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr. 1969;14:454–8.
Watsuji T, Yamamoto A, Takaki Y, Ueda K, Kawagucci S, Takai K. Diversity and methane oxidation of active epibiotic methanotrophs on live Shinkaia crosnieri. ISME J. 2014;8:1020–31.
pubmed: 24401859
pmcid: 3996700
Watsuji T, Motoki K, Hada E, Nagai Y, Takaki Y, Yamamoto A, et al. Compositional and functional shifts in the epibiotic bacterial community of Shinkaia crosnieri Baba & Williams (a squat lobster from hydrothermal vents) during methane-fed rearing. Microbes Environ. 2018;33:348–56.
pubmed: 30333383
pmcid: 6308002
DeLong EF. Archaea in coastal marine environments. Proc Natl Acad Sci USA. 1992;89:5685–9.
pubmed: 1608980
Pham VH, Yong JJ, Park SJ, Yoon DN, Chung WH, Rhee SK. Molecular analysis of the diversity of the sulfide:quinone reductase (sqr) gene in sediment environments. Environ Microbiol. 2008;154:3112–21.
Sanger F, Nicklen EF, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA. 1977;74:5463–7.
pubmed: 271968
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71.
pubmed: 14985472
pmcid: 390282
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–9.
pubmed: 21546353
pmcid: 3203626
Miyazaki J, Higa R, Toki T, Ashi J, Tsunogai U, Nunoura T, et al. Molecular characterization of potential nitrogen fixation by anaerobic methane-oxidizing archaea in the methane seep sediments at the number 8 Kumano Knoll in the Kumano Basin, offshore of Japan. Appl Environ Microbiol. 2009;75:7153–62.
pubmed: 19783748
pmcid: 2786543
Hongo Y, Ikuta T, Takaki Y, Shimamura S, Shigenobu S, Maruyama T, et al. Expression of genes involved in the uptake of inorganic carbon in the gill of a deep-sea vesicomyid clam harboring intracellular thioautotrophic bacteria. Gene. 2016;585:228–40.
pubmed: 27016297
Takishita K, Takaki Y, Chikaraishi Y, Ikuta T, Ozawa G, Yoshida T, et al. Genomic evidence that methanotrophic endosymbionts likely provide deep-sea Bathymodiolus mussels with a sterol intermediate in cholesterol biosynthesis. Genome Biol Evol. 2017;9:1148–60.
pubmed: 28453654
pmcid: 5421315
Wakai S, Kikumoto M, Kanao T, Kamimura K. Involvement of sulfide:quinone oxidoreductase in sulfur oxidation of an acidophilic iron-oxidizing bacterium, Acidithiobacillus ferrooxidans NASF-1. Biosci Biotechnol Biochem. 2004;68:2519–28.
pubmed: 15618623
Beedessee G, Watanabe H, Ogura T, Nemoto S, Yahagi T, Nakagawa S, et al. High connectivity of animal populations in deep-sea hydrothermal vent fields in the Central Indian Ridge relevant to its geological setting. PLoS One. 2013;8:e81570.
pubmed: 24358117
pmcid: 3864839
Warén A, Bengtson S, Goffredi SK, Van Dover CL. A hot-vent gastropod with iron sulfide dermal sclerites. Science. 2003;302:1007–7.
pubmed: 14605361
Chen C, Linse K, Copley JT, Rogers AD. The “scaly-foot gastropod”: a new genus and species of hydrothermal vent-endemic gastropod (Neomphalina: Peltospiridae) from the Indian Ocean. J Molluscan Stud. 2015;81:322–34.
Takai K, Nunoura T, Ishibashi J, Lupton J, Suzuki R, Hamasaki H, et al. Variability in the microbial communities and hydrothermal fluid chemistry at the newly-discovered Mariner hydrothermal field, southern Lau Basin. J Geophys Res. 2008;113:G02031.
Yamamoto M, Takai K. Sulfur metabolisms in Epsilon- and Gamma-proteobacteria in deep-Sea hydrothermal fields. Front Microbiol. 2011;2. https://doi.org/10.3389/fmicb.2011.00192 .
Cusick KD, Fitzgerald LA, Cockrell AL, Biffinger JC. Selection and evaluation of reference genes for reverse transcription-quantitative PCR expression studies in a thermophilic bacterium grown under different culture conditions. PLoS One. 2015;10:e0131015.
pubmed: 26115538
pmcid: 4482720
Zhao W, Li Y, Gao P, Sun Z, Sun T, Zhang H. Validation of reference genes for real-time quantitative PCR studies in gene expression levels of Lactobacillus casei Zhang. J Ind Microbiol Biotechnol. 2010;38:1279–86.
Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002;30:e36.
pubmed: 11972351
pmcid: 113859
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3:RESEARCH0034.
pubmed: 12184808
pmcid: 126239
Beinart RA, Nyholm SV, Dubilier N, Girguis PR. Intracellular oceanospirillales inhabit the gills of the hydrothermal vent snail Alviniconcha with chemosynthetic, γ-proteobacterial symbionts. Environ Microbiol Rep. 2014;6:656–64.
pubmed: 25756119
Mitchell JH, Leonard JM, Delaney J, Girguis PR, Scott KM. Hydrogen does not appear to be a major electron donor for symbiosis with the deep-sea hydrothermal vent tubeworm Riftia pachyptila. Appl Environ Microbiol. 2019;86:e01522–19. https://doi.org/10.1128/AEM.01552-19 .
doi: 10.1128/AEM.01552-19
pubmed: 31628148