Microbial biodiversity in glacier-fed streams

ISME Journal

Volumn 7, Issue 8, 2013, Pages 1651-1660

  Wilhelm, Linda ^a   Singer, Gabriel A ^a,b   Fasching, Christina ^a   Battin, Tom J ^a,b   Besemer, Katharina ^a,b  

^a UNIVERSITY OF VIENNA   (Austria)

^b Aquatic Lipid Research and Ecotoxicology   (Austria)

Author keywords

Biofilm; Climate change; Glacier fed streams; Metacommunity ecology; Microbial diversity

Indexed keywords

RNA 16S;

BACTERIUM; BIOFILM; BIOGEOCHEMISTRY; CHLOROPLAST; COMMUNITY COMPOSITION; COMMUNITY ECOLOGY; CYANOBACTERIUM; DOMINANCE; ELEVATION; ENVIRONMENTAL CONDITIONS; GENETIC ANALYSIS; GLACIER DYNAMICS; GLACIER RETREAT; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; SPECIES DIVERSITY; STREAMWATER; VALLEY GLACIER;

ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BIODIVERSITY; BIOFILM; CLASSIFICATION; ENVIRONMENT; GENETICS; ICE COVER; MICROBIOLOGY; RIVER;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODIVERSITY; BIOFILMS; ENVIRONMENT; ICE COVER; RIVERS; RNA, RIBOSOMAL, 16S; WATER MICROBIOLOGY;

ACTINOBACTERIA; BACTEROIDETES; PROTEOBACTERIA;

EID: 84880919522     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.44     Document Type: Article

References (117)

1. Anderson MJ, Ellingsen KE, Mcardle BH. (2006a). Multivariate dispersion as a measure of beta diversity. Ecol Lett 9: 683-693.
2. Anderson MJ. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
3. Anderson MJ. (2006b). Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245-253.
4. Anesio AM, Laybourn-Parry J. (2012). Glaciers and ice sheets as a biome. Trends Ecol Evol 27: 219-225.
5. Bardgett RD, Richter A, Bol R, Garnett MH, Bäumler R, Xu X et al. (2007). Heterotrophic microbial communities use ancient carbon following glacial retreat. Biol Lett 3: 487-490.
6. Battin JT, Wille A, Psenner R, Richter A. (2004). Largescale environmental controls on microbial biofilms in high-alpine streams. Biogeoscience 1: 159-171.
7. Battin TJ, Kaplan LA, Findlay S, Hopkinson CS, Marti E, Packman AI et al. (2008). Biophysical controls on organic carbon fluxes in fluvial networks. Nat Geosci 1: 95-100.
8. Berry D, Mahfoudh KB, Wagner M, Loy A. (2011). Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl Environ Microbiol 77: 7846-7849.
9. Besemer K, Peter H, Logue JB, Langenheder S, Lindström ES, Tranvik LJ et al. (2012). Unraveling assembly of stream biofilm communities. ISME J 6: 1459-1468.
10. Blanchet FG, Legendre P, Borcard D. (2008). Forward selection of explanatory variables. Ecology 89: 2623-2632.
11. Brown LE, Hannah DM, Milner AM. (2003). Alpine stream habitat classification: An alternative approach incorporating the role of dynamic water source contributions. Arct Antarct Alp Res 35: 313-322.
12. Brown LE, Hannah DM, Milner AM. (2007a). Vulnerability of alpine stream biodiversity to shrinking glaciers and snowpacks. Glob Change Biol 13: 958-966.
13. Brown LE, Milner AM, Hannah DM. (2007b). Groundwater influence on alpine stream ecosystems. Freshwater Biol 52: 878-890.
14. Cheng SM, Foght JM. (2007). Cultivation-independent and -dependent characterization of bacteria resident beneath John Evans Glacier. FEMS Microbiol Ecol 59: 318-330.
15. Cleveland WS, Grosse E, Shyu WM. (1992). Local regression models. Chambers JM, Hastie TJ (eds) Statistical Models in S. Wadsworth & Brooks/Cole, Pacific Grove, CA, USA.
16. Edwards A, Anesio AM, Rassner SM, Sattler B, Hubbard B, Perkins WT et al. (2011). Possible interactions between bacterial diversity, microbial activity and supraglacial hydrology of cryoconite holes in Svalbard. ISME J 5: 150-160.
17. Fierer N, Jackson RB. (2006). The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci 103: 626-631.
18. Finn DS, Bonada N, Mú rria C, Hughes JM. (2011). Small but mighty: Headwaters are vital to stream network biodiversity at two levels of organization. J N Am Benthol Soc 30: 963-980.
19. Finn DS, Khamis K, Milner AM. (2012). Loss of small glaciers will diminish beta diversity in Pyrenean streams at two levels of biological organization. Global Ecol Biogeogr 22: 40-51.
20. Finn DS, Räsänen K, Robinson CT. (2010). Physical and biological changes to a lengthening stream gradient following a decade of rapid glacial recession. Glob Change Biol 16: 3314-3326.
21. Goslee SC, Urban DL. (2007). The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22: 1-19.
22. Hannah DM, Brown LE, Milner AM, Gurnell AM, McGregor GR, Petts GE et al. (2007). Integrating climate-hydrology-ecology for alpine river systems. Aquatic Conserv: Mar Freshw Ecosyst 17: 636-656.
23. Hervas A, Casamayor EO. (2009). High similarity between bacterioneuston and airborne bacterial community compositions in a high mountain lake area. FEMS Microbiol Ecol 67: 219-228.
24. Hodson A, Anesio AM, Tranter M, Fountain A, Osborn M, Priscu J et al. (2008). Glacial ecosystems. Ecol Monogr 78: 41-67.
25. Hughes JM, Schmidt DJ, Finn DS. (2009). Genes in streams: Using DNA to understand the movement of freshwater fauna and their riverine habitat. Bioscience 59: 573-583.
26. Hullar MAJ, Kaplan LA, Stahl DA. (2006). Recurring seasonal dynamics of microbial communities in stream habitats. Appl Environ Microbiol 72: 713-722.
27. Jacobsen D, Dangles O. (2011). Environmental harshness and global richness patterns in glacier-fed streams. Global Ecol Biogeogr 21: 647-656.
28. Jacobsen D, Milner AM, Brown LE, Dangles O. (2012). Biodiversity under threat in glacier-fed river systems. Nature Clim Change 2: 361-364.
29. Legendre P, Oksanen J, Braak CFJ. (2011). Testing the significance of canonical axes in redundancy analysis. Methods Ecol Evol 2: 269-277.
30. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF et al. (2004). The metacommunity concept: A framework for multi-scale community ecology. Ecol Lett 7: 601-613.
31. Lichstein JW. (2006). Multiple regression on distance matrices: A multivariate spatial analysis tool. Plant Ecol 188: 117-131.
32. Loveland-Curtze J, Miteva VI, Brenchley JE. (2009). Herminiimonas glaciei sp. nov., a novel ultramicrobacterium from 3042 m deep Greenland glacial ice. Int J Syst Evol Microbiol 59: 1272-1277.
33. Milner AM, Brown LE, Hannah DM. (2009). Hydroecological response of river systems to shrinking glaciers. Hydrol Process 23: 62-77.
34. Murdoch D, Chow ED. (2007). Ellipse: Functions for drawing ellipses and ellipse-like confidence regions. R Package Version 0.3 - 5.
35. Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara RB, Simpson GL et al. (2011). Vegan: Community Ecology Package. R Package Version 1.17-11.
36. Ptacnik R, Andersen T, Brettum P, LepistöL, Willén E. (2010). Regional species pools control community saturation in lake phytoplankton. Proc R Soc B 277: 3755-3764.
37. Quince C, Curtis TP, Sloan WT. (2008). The rational exploration of microbial diversity. ISME J 2: 997-1006.
38. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ. (2011). Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38.
39. R Development Core Team (2011). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, A.T.
40. Schütte UME, Abdo Z, Foster J, Ravel J, Bunge J, Solheim B et al. (2010). Bacterial diversity in a glacier foreland of the high Arctic. Mol Ecol 19: 54-66.
41. Sichel H. (1974). On a distribution representing sentencelength in written prose. J R Stat Soc A 137: 25-34.
42. Simon C, Wiezer A, Strittmatter AW, Daniel R. (2009). Phylogenetic diversity and metabolic potential revealed in a glacier ice metagenome. Appl Environ Microbiol 75: 7519-7526.
43. Singer GA, Fasching C, Wilhelm L, Niggemann J, Steier P, Dittmar T et al. (2012). Biogeochemically diverse organic matter in Alpine glaciers and its downstream fate. Nature Geosci 5: 710-714.
44. Tamames J, Abellán JJ, Pignatelli M, Camacho A, Moya A. (2010). Environmental distribution of prokaryotic taxa. BMC Microbiol 10: 85.
45. Vincent WF. (2010). Microbial ecosystem responses to rapid climate change in the Arctic. ISME J 4: 1089-1091.
46. Wang Q, Garrity GM, Tiedje JM, Cole Jr. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267
47. Ward JV, Tockner K, Arscott DB, Claret C. (2002). Riverine landscape diversity. Freshwater Biol 47: 517-539.
48. Warnes GR, Bolker B, Gorjanc G, Grothendieck G, Korosec A, Lumley T et al. (2011). gdata: Various R programming tools for data manipulation. R Package Version 2.8.2.
49. Woodward G, Perkins DM, Brown LE. (2010). Climate change and freshwater ecosystems: Impacts across multiple levels of organization. Phil Trans R Soc B 365: 2093-2106.
50. Xiang S, Shang T, Chen Y, Jing Z, Yao T. (2009). Dominant bacteria and biomass in the Kuytun 51 Glacier. Appl Environ Microbiol 75: 7287-7290.
51. Anderson JK, Smith TG, Hoover TR. (2010). Sense and sensibility: Flagellum-mediated gene regulation. Trends Microbiol 18: 30-37.
52. Beinart RA, Sanders JG, Faure B, Sylva SP, Lee RW, Becker EL et al. (2012). Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses. Proc Natl Acad Sci USA 109: E3241-E3250.
53. Berg I. (2011). Ecological aspects of the distribution of different autotrophic CO2 fixation pathways. Appl Environ Microbiol 77: 1925-1936.
54. Berks B. (1995). Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochim Biophys Acta 1232: 97-173.
55. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Meth 7: 335-336.
56. Childress JJ, Fisher CR, Brooks JM, Kennicutt MC, Bidigare R, Anderson AE. (1986). A methanotrophic marine molluscan (bivalvia, mytilidae) symbiosis: Mussels fueled by gas. Science 233: 1306-1308.
57. Childress JJ, Fisher CR, Favuzzi JA, Sanders NK. (1991). Sulfide and carbon dioxide uptake by the hydrothermal vent clam, Calyptogena magnifica, and its chemoautotrophic symbionts. Physiol Zool 64: 1444-1470.
58. Childress JJ, Girguis PR. (2011). The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities. J Exp Biol 214: 312-325.
59. Dowd S, Callaway T, Wolcott R, Sun Y, McKeehan T, Hagevoort R et al. (2008). Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8: 125.
60. Dubilier N, Bergin C, Lott C. (2008). Symbiotic diversity in marine animals: The art of harnessing chemosynthesis. Nat Rev Micro 6: 725-740.
61. Edgar RC. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
62. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
63. Felbeck H. (1981). Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila jones (Vestimentifera). Science 213: 336-338.
64. Fisher CR, Childress JJ. (1984). Substrate Oxidation by Trophosome Tissue from Riftia pachyptila Jones (Phylum pogonophora vol. 5. Elsevier: Amsterdam, PAYS-BAS.
65. Frigaard N-U, Dahl C. (2009). Sulfur Metabolism in phototrophic sulfur bacteria. Adv Microb Physiol 54: 103-200.
66. Gardebrecht A, Markert S, Sievert SM, Felbeck H, Thurmer A, Albrecht D et al. (2012). Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics. ISME J 6: 766-776.
67. Ghosh W, Dam B. (2009). Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol Rev 33: 999-1043.
68. Girguis PR, Childress JJ. (2006). Metabolite uptake, stoichiometry and chemoautotrophic function of the hydrothermal vent tubeworm Riftia pachyptila: Responses to environmental variations in substrate concentrations and temperature. J Exp Biol 209: 3516-3528.
69. Gomez-Alvarez V, Teal TK, Schmidt TM. (2009). Systematic artifacts in metagenomes from complex microbial communities. ISME J 3: 1314-1317.
70. Gracey AY. (2007). Interpreting physiological responses to environmental change through gene expression profiling. J Exp Biol 210: 1584-1592.
71. Gracey AY, Chaney ML, Boomhower JP, Tyburczy WR, Connor K, Somero GN. (2008). Rhythms of gene expression in a fluctuating intertidal environment. Curr Biol 18: 1501-1507.
72. Grimm F, Franz B, Dahl C. (2008). Thiosulfate and Sulfur Oxidation in Purple Sulfur Bacteria Microbial Sulfur Metabolism In: Dahl C, Friedrich CG (eds).Springer: Berlin Heidelberg, pp 101-116.
73. Harada M, Yoshida T, Kuwahara H, Shimamura S, Takaki Y, Kato C et al. (2009). Expression of genes for sulfur oxidation in the intracellular chemoautotrophic symbiont of the deep-sea bivalve Calyptogena okutanii. Extremophiles 13: 895-903.
74. Harmer TL, Rotjan RD, Nussbaumer AD, Bright M, Ng AW, DeChaine EG et al. (2008). Free-living tube worm endosymbionts found at deep-sea vents. Appl Environ Microbiol 74: 3895-3898.
75. Hentschel U, Felbeck H. (1993). Nitrate respiration in the hydrothermal vent tubeworm Riftia pachyptila. Nature 366: 338-340.
76. 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: 427-433.
77. Hugler M, Wirsen CO, Fuchs G, Taylor CD, Sievert SM. (2005). Evideince for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle by members of the epsilon subdivision of Proteobacteria. J Bacteriol 187: 3020-3027.
78. Huson DH, Mitra S, Ruscheweyh H-J, Weber N, Schuster SC. (2011). Integrative analysis of environmental sequences using MEGAN4. Genome Res 21: 1552-1560.
79. Hügler M, Petersen JM, Dubilier N, Imhoff JF, Sievert SM. (2011). Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS One 6: E16018.
80. Johnson KS, Beehler CL, Sakamoto-Arnold CM, Childress JJ. (1986). In situ measurements of chemical distributions in a deep-sea hydrothermal vent field. Science 231: 1139-1141.
81. Kuwahara H, Yoshida T, Takaki Y, Shimamura S, Nishi S, Harada M et al. (2007). Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr Biol 17: 881-886.
82. 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: 289-300.
83. Maezawa K, Shigenobu S, Taniguchi H, Kubo T, Aizawa S-i, Morioka M. (2006). Hundreds of flagellar basal bodies cover the cell surface of the endosymbiotic bacterium Buchnera aphidicola sp. strain APS. J Bacteriol 188: 6539-6543.
84. Markert S, Gardebrecht A, Felbeck H, Sievert SM, Klose J, Becher D et al. (2011). Status quo in physiological proteomics of the uncultured Riftia pachyptila endosymbiont. Proteomics 11: 3106-3117.
85. Meyer F, Paarmann D, D'Souza M, Olson R, Glass E, Kubal M et al. (2008). The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9: 386.
86. Millikan DS, Ruby EG. (2004). Vibrio fischeri flagellin A is essential for normal motility and for symbiotic competence during initial squid light organ colonization. J Bacteriol 186: 4315-4325.
87. Moran NA, Plague GR. (2004). Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14: 627-633.
88. Mottl MJ, Seewald JS, Wheat CG, Tivey MK, Michael PJ, Proskurowski G et al. (2011). Chemistry of hot springs along the Eastern Lau Spreading Center. Geochimica Et Cosmochimica Acta 75: 1013-1038.
89. Nakagawa S, Takai K. (2008). Deep-sea vent chemoautotrophs: Diversity, biochemistry and ecological significance. FEMS Microbiol Ecol 65: 1-14.
90. Nakagawa S, Takai K, Inagaki F, Hirayama H, Nunoura T, Horikoshi K et al. (2005). Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environ Microbiol 7: 1619-1632.
91. Newton ILG, Woyke T, Auchtung TA, Dilly GF, Dutton RJ, Fisher MC et al. (2007). The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315: 998-1000.
92. Nyholm SV, Stabb EV, Ruby EG, McFall-Ngai MJ. (2000). Establishment of an animal-bacterial association: Recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci 97: 10231-10235.
93. Petersen JM, Zielinski FU, Pape T, Seifert R, Moraru C, Amann R et al. (2011). Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476: 176-180.
94. Potter L, Angove H, Richardson D, Cole J. (2001). Nitrate reduction in the periplasm of gram-negative bacteria. Adv Microb Physiol 45: 51-112.
95. Potter LC, Millington P, Griffiths L, Thomas GH, Cole JA. (1999). Competition between Escherichia coli strains expressing either a periplasmic or a membranebound nitrate reductase: Does Nap confer a selective advantage during nitrate-limited growth? Biochem J 344: 77-84.
96. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies Jr et al. (2007). SILVA: A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
97. Reeder J, Knight R. (2010). Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Meth 7: 668-669.
98. Reitzer L. (2003). Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 57: 155-176.
99. Robidart JC, Bench SR, Feldman RA, Novoradovsky A, Podell SB, Gaasterland T et al. (2008). Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ Microbiol 10: 727-737.
100. Robidart JC, Roque A, Song P, Girguis PR. (2011). Linking hydrothermal geochemistry to organismal physiology: Physiological versatility in Riftia pachyptila from sedimented and basalt-hosted vents. PLoS One 6: E21692.
101. Sievert SM, Scott KM, Klotz MG, Chain PSG, Hauser LJ, Hemp J et al. (2008). Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl Environ Microbiol 74: 1145-1156.
102. Sievert SM, Vetriani C. (2012). Chemoautotrophy at deepsea vents: Past, present, and future. Oceanography 25: 218-233.
103. Sikorski J, Munk C, Lapidus C, Djao ODN, Lucas S, Glavina Del Rio T et al. (2010). Complete genome sequence of Sulfurimonas autotrophica type strain (OK10). Stand Genomic Sci 3: 194-202.
104. Stewart F, Dmytrenko O, DeLong E, Cavanaugh C. (2011). Metatranscriptomic analysis of sulfur oxidation genes in the endosymbiont of Solemya velum. Front Microbiol 2: 134.
105. Stewart FJ, Newton ILG, Cavanaugh CM. (2005). Chemosynthetic endosymbioses: Adaptations to oxic-anoxic interfaces. Trends Microbiol 13: 439-448.
106. Stewart FJ, Ottesen EA, DeLong EF. (2010). Development and quantitative analyses of a universal rRNA-subtraction protocol for microbial metatranscriptomics. ISME J 4: 896-907.
107. Suzuki Y, Kojima S, Sasaki T, Suzuki M, Utsumi T, Watanabe H et al. (2006). Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Appl Environ Microbiol 72: 1388-1393.
108. Suzuki Y, Sasaki T, Suzuki M, Nogi Y, Miwa T, Takai K et al. (2005). Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl Environ Microbiol 71: 5440-5450.
109. Takai K, Campbell BJ, Cary SC, Suzuki M, Oida H, Nunoura T et al. (2005). Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of epsilonproteobacteria. Appl Environ Microbiol 71: 7310-7320.
110. Takai K, Suzuki M, Nakagawa S, Miyazaki M, Suzuki Y, Inagaki F et al. (2006). Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfuroxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int J Syst Evol Micr 56: 1725-1733.
111. Tivey MK. (2007). Generation of seafloor hydrothermal vent fluids and associated mineral deposits. Oceanography 20: 50-65.
112. Toft C, Fares MA. (2008). The evolution of the flagellar assembly pathway in endosymbiotic bacterial genomes. Mol Biol Evol 25: 2069-2076.
113. Vignais PM, Billoud B. (2007). Occurrence, classification, and biological function of hydrogenases: An overview. Chem Rev 107: 4206-4272.
114. Wendeberg A, Zielinski FU, Borowski C, Dubilier N. (2012). Expression patterns of mRNAs for methanotrophy and thiotrophy in symbionts of the hydrothermal vent mussel Bathymodiolus puteoserpentis. ISME J 6: 104-112.
115. Wittenberg JB, Stein JL. (1995). Hemoglobin in the symbiont-harboring gill of the marine gastropod Alviniconcha hessleri. Biol Bull 188: 5-7.
116. Woyke T, Teeling H, Ivanova NN, Huntemann M, Richter M, Gloeckner FO et al. (2006). Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443: 950-955.
117. Yamamoto M, Takai K. (2011). Sulfur metabolisms in epsilon- and gamma-Proteobacteria in deep-sea hydrothermal fields. Front Microbiol 2192.