Sunken woods on the ocean floor provide diverse specialized habitats for microorganisms

FEMS Microbiology Ecology

Volumn 82, Issue 3, 2012, Pages 616-628

  Fagervold, Sonja K ^a,b   Galand, Pierre E ^a,b   Zbinden, Magali ^d   Gaill, Françoise ^d,e   Lebaron, Philippe ^a,c   Palacios, Carmen ^a,f,g  

^a SORBONNE UNIVERSITÉ   (France)

^b Observatoire Océanologique de Banyuls sur Mer   (France)

^c Laboratoire d Océanographie Microbienne   (France)

^d Systematique Adaptations et Evolution ^*  (France)

^e Institut Ecologie et Environnement   (France)

^f UMR 5110   (France)

^g IFREMER   (France)

Author keywords

Chemosynthetic marine environments; Marine microbial diversity; Marine woodfalls; Phylogenetic community structure

Indexed keywords

RNA 16S; SEA WATER;

BACTERIUM; BIOMASS; CHEMOAUTOTROPHY; COMMUNITY STRUCTURE; GEOGRAPHICAL REGION; MARINE ECOSYSTEM; MICROBIAL COMMUNITY; ORGANIC MATTER; PHYLOGENETICS; SEAFLOOR; WOOD;

ARCHAEON; ARTICLE; BACTERIUM; BIOMASS; CLASSIFICATION; ECOSYSTEM; EURYARCHAEOTA; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; SEA;

ARCHAEA; BACTERIA; BIOMASS; ECOSYSTEM; EURYARCHAEOTA; OCEANS AND SEAS; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEAWATER;

ARCHAEA; BACTERIA (MICROORGANISMS);

EID: 84869861717     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2012.01432.x     Document Type: Article

References (82)

1. Abram JW & Nedwell DB (1978) Hydrogen as a substrate for methanogenesis and sulphate reduction in anaerobic saltmarsh sediment. Arch Microbiol 117: 93-97.
2. Amaral-Zettler LA, Zettler ER, Theroux SM, Palacios C, Aguilera A & Amils R (2011) Microbial community structure across the tree of life in the extreme Rio Tinto. ISME J 5: 42-50.
3. Ander P & Eriksson K-E (1985) Methanol formation during lignin degradation by Phanerochaete chrysosporium Appl Microbiol Biotechnol 21: 96-102.
4. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ & Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71: 7724-7736.
5. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ & Weightman AJ (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72: 5734-5741.
6. Barberán A & Casamayor EO (2010) Global phylogenetic community structure and beta-diversity patterns in surface bacterioplankton metacommunities. Aquat Microb Ecol 59: 1-10.
7. Barbeyron T, L'Haridon S, Corre E, Kloareg B & Potin P (2001) Zobellia galactanovorans gen. nov., sp. nov., a marine species of Flavobacteriaceae isolated from a red alga, and classification of [Cytophaga] uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Zobellia uliginosa gen. nov., comb. nov. Int J Syst Evol Microbiol 51: 985-997.
8. Bennett BA, Smith CR, Glaser B & Maybaum HL (1994) Community structure of a chemoautotrophic assemblage on whale bones in the deep northeast Pacific Ocean. Mar Ecol Prog Ser 108: 205-223.
9. Bowman JP (2006) The marine clade of the family Flavobacteriaceae: the genera Aequorivita, Arenibacter, Cellulophaga, Croceibacter, Formosa, Gelidibacter, Gillisia, Maribacter, Mesonia, Muricauda, Polaribacter, Psychroflexus, Psychroserpens, Robiginitalea, Salegentibacter, Tenacibaculum, Ulvibacter, Vitellibacter and Zobellia Prokaryotes 7: 677-694.
10. Bowman JP & McCuaig RD (2003) Biodiversity, community structural shifts, and biogeography of Prokaryotes within Antarctic continental shelf sediment. Appl Environ Microbiol 69: 2463-2483.
11. Burggraf S, Olsen GJ, Stetter KO & Woese CR (1992) A phylogenetic analysis of Aquifex pyrophilus Syst Appl Microbiol 15: 352-356.
12. Chou H-H & Holmes MH (2001) DNA sequence quality trimming and vector removal. Bioinformatics 17: 1093-1104.
13. Clausen CA (1996) Bacterial associations with decaying wood: a review. Int Biodeterior Biodegradation 37: 101-107.
14. Cottrell MT & Kirchman DL (2000) Natural assemblages of marine Proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66: 1692-1697.
15. Deming JW, Reysenbach A-L, Macko SA & Smith CR (1997) Evidence for the microbial basis of a chemoautotrophic invertebrate community at a whale fall on the deep seafloor: bone-colonizing bacteria and invertebrate endosymbionts. Microsc Res Tech 37: 162-170.
16. Distel DL, Baco AR, Chuang E, Morrill W, Cavanaugh C & Smith CR (2000) Marine ecology: do mussels take wooden steps to deep-sea vents? Nature 403: 725-726.
17. Distel DL, Morrill W, MacLaren-Toussaint N, Franks D & Waterbury J (2002) Teredinibacter turnerae gen. nov., sp. nov., a dinitrogen-fixing, cellulolytic, endosymbiotic gamma-proteobacterium isolated from the gills of wood-boring molluscs (Bivalvia: Teredinidae). Int J Syst Evol Microbiol 52: 2261-2269.
18. Donnelly MI & Dagley S (1980) Production of methanol from aromatic acids by Pseudomonas putida J Bacteriol 142: 916-924.
19. Dubinina G, Grabovich M, Leshcheva N, Rainey FA & Gavrish E (2011) Spirochaeta perfilievii sp. nov., oxygen-tolerant, sulfide oxidizing, sulfur and thiosulfate-reducing spirochete isolated from a saline spring. Int J Syst Evol Microbiol 61: 110-117.
20. Duperron S, Laurent MCZ, Gaill F & Gros O (2008) Sulphur-oxidizing extracellular bacteria in the gills of Mytilidae associated with wood falls. FEMS Microbiol Ecol 63: 338-349.
21. Eder W, Jahnke LL, Schmidt M & Huber R (2001) Microbial diversity of the brine-seawater interface of the Kebrit Deep, Red Sea, studied via 16S rRNA gene sequences and cultivation methods. Appl Environ Microbiol 67: 3077-3085.
22. Ewing B, Hillier L, Wendl M & Green P (1998) Basecalling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8: 175-185.
23. Felsenstein J (1993) PHYLIP (Phylogenetic Inference Package) Version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle, WA.
24. Finster K (2008) Microbiological disproportionation of inorganic sulfur compounds. J Sulfur Chem 29: 281-292.
25. Gareth Jones EB, Turner RD, Furtado SEJ & Kuhne H (1976) Marine deteriogenic organisms 1. Lignicolous fungi and bacteria and the wood boring mollusca and crustacea. Int Biodeterior Bull 12: 120-134.
26. Goffredi SK & Orphan VJ (2010) Bacterial community shifts in taxa and diversity in response to localized organic loading in the deep sea. Environ Microbiol 12: 344-363.
27. Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T, Turk K, Lee R & Vrijenhoek RC (2005) Evolutionary innovation: a bone-eating marine symbiosis. Environ Microbiol 7: 1369-1378.
28. Goffredi SK, Wilpiszeski R, Lee R & Orphan VJ (2008) Temporal evolution of methane cycling and phylogenetic diversity of archaea in sediments from a deep-sea whale-fall in Monterey Canyon, California. ISME J 2: 204-220.
29. Grunke S, Felden J, Lichtschlag A, Girnth AC, De Beer D, Wenzhofer F & Boetius A (2011) Niche differentiation among mat-forming, sulfide-oxidizing bacteria at cold seeps of the Nile Deep Sea Fan (Eastern Mediterranean Sea). Geobiology 9: 330-348.
30. Herrera CM, Canto A, Pozo MAI & Bazaga P (2010) Inhospitable sweetness: nectar filtering of pollinator-borne inocula leads to impoverished, phylogenetically clustered yeast communities. Proc Biol Sci 277: 747-754.
31. Horner-Devine MC & Bohannan BJM (2006) Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87: S100-S108.
32. Horner-Devine MC, Silver JM, Leibold MA et al. (2007) A comparison of taxon co-occurrence patterns for macro- and microorganisms. Ecology 88: 1345-1353.
33. Iizuka T, Jojima Y, Fudou R & Yamanaka S (1998) Isolation of myxobacteria from the marine environment. FEMS Microbiol Lett 169: 317-322.
34. Inagaki F, Suzuki M, Takai K, Oida H, Sakamoto T, Aoki K, Nealson KH & Horikoshi K (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl Environ Microbiol 69: 7224-7235.
35. Isenbarger TA, Finney M, Rios-Velazquez C, Handelsman J & Ruvkun G (2008) Miniprimer PCR, a new lens for viewing the microbial world. Appl Environ Microbiol 74: 840-849.
36. Jorgensen BB & Boetius A (2007) Feast and famine; microbial life in the deep-sea bed. Nat Rev Microbiol 5: 770-781.
37. Jurgens JA, Blanchette RA & Carlson DN (2003) Evaluating the wooden remnants of Tektas Burnu shipwreck. Art, Biology and Conservation: Biodeterioration of Works of Art ( Koestler RJ, Koestler VH, Charola AE & Nieto-Fernandez FE, eds), pp. 390-407. Metropolitan Museum of Art, New York.
38. Khelaifia S, Fardeau M-L, Pradel N, Aussignargues C, Garel M, Tamburini C, Cayol J-L, Gaudron S, Gaill F & Ollivier B (2011) Desulfovibrio piezophilus sp. nov., a piezophilic, sulfate-reducing bacterium isolated from wood falls in the Mediterranean Sea. Int J Syst Evol Microbiol 61: 2706-2711.
39. Kirchman DL (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39: 91-100.
40. Knittel K, Boetius A, Lemke A, Eilers H, Lochte K, Pfannkuche O, Linke P & Amann R (2003) Activity, distribution, and diversity of sulfate reducers and other bacteria in sediments above gas hydrate (Cascadia Margin, Oregon). Geomicrobiol J 20: 269-294.
41. Kohlmeyer J (1978) Bacterial attack on wood and cellophane in the deep sea. International Biodeterioration Symposium, Vol. 4 ( Oxley TA, Becker G & Allsopp D, eds), pp. 187-192. Berlin.
42. Landy ET, Mitchell JI, Hotchkiss S & Eaton RA (2008) Bacterial diversity associated with archaeological waterlogged wood: ribosomal RNA clone libraries and denaturing gradient gel electrophoresis (DGGE). Int Biodeterior Biodegradation 61: 106-116.
43. Laurent MCZ, Gros O, Brulport J-P, Gaill F & LeBris N (2009) Sunken wood habitat for thiotrophic symbiosis in mangrove swamps. Mar Environ Res 67: 83-88.
44. Leschine SB (1995) Cellulose degradation in anaerobic environments. Annu Rev Microbiol 49: 399-426.
45. Letunic I & Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23: 127-128.
46. Lorion J, Duperron S, Gros O, Cruaud C & Samadi S (2009) Several deep-sea mussels and their associated symbionts are able to live both on wood and on whale falls. Proc Biol Sci 276: 177-185.
47. Lovley DR, Dwyer DF & Klug MJ (1982) Kinetic analysis of competition between sulfate reducers and methanogens for hydrogen in sediments. Appl Environ Microbiol 43: 1373-1379.
48. Ludwig W, Strunk O, Westram R et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
49. Martin AP (2002) Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl Environ Microbiol 68: 3673-3682.
50. Mouzouras R, Gareth Jones EB, Venkatasamy R & Holt DM (1988) Microbial decay of lignicellulose in the marine environment. Marine Biodeteriation Advaced Techniques Applicable to the Indian Ocean ( Thompson M-F, Sarojini R & Nagabhushanam R, eds), pp. 345-356. A.A. Balkema, Rotterdam.
51. Na H, Kim S, Moon EY & Chun J (2009) Marinifilum fragile gen. nov., sp. nov., isolated from tidal flat sediment. Int J Syst Evol Microbiol 59: 2241-2246.
52. Nogi Y, Kato C & Horikoshi K (2002) Psychromonas kaikoae sp. nov., a novel piezophilic bacterium from the deepest cold-seep sediments in the Japan Trench. Int J Syst Evol Microbiol 52: 1527-1532.
53. Ojeda F, Pausas J & Verdù M (2010) Soil shapes community structure through fire. Oecologia 163: 729-735.
54. Oremland RS & Taylor BF (1978) Sulfate reduction and methanogenesis in marine sediments. Geochim Cosmochim Acta 42: 209-214.
55. Oremland RS, Marsh LM & Polcin S (1982) Methane production and simultaneous sulphate reduction in anoxic, salt marsh sediments. Nature 296: 143-145.
56. Orphan VJ, Hinrichs K-U, Ussler W III, Paull CK, Taylor LT, Sylva SP, Hayes JM & Delong EF (2001) Comparative analysis of methane-oxidizing archaea and sulfate-reducing bacteria in anoxic marine sediments. Appl Environ Microbiol 67: 1922-1934.
57. Pachiadaki MG, Lykousis V, Stefanou EG & Kormas KA (2010) Prokaryotic community structure and diversity in the sediments of an active submarine mud volcano (Kazan mud volcano, East Mediterranean Sea). FEMS Microbiol Ecol 72: 429-444.
58. Pachiadaki M, Kallionaki A, Dählmann A, De Lange G & Kormas K (2011) Diversity and spatial distribution of prokaryotic communities along a sediment vertical profile of a Deep-Sea mud volcano. Microb Ecol 62: 655-668.
59. Palacios C, Zettler E, Amils R & Amaral-Zettler L (2008) Contrasting microbial community assembly hypotheses: a reconciling tale from the Rio Tinto. PLoS ONE 3: e3853.
60. Palacios C, Zbinden M, Pailleret M, Gaill F & Lebaron P (2009) Highly similar prokaryotic communities of sunken wood at shallow and Deep-Sea sites across the oceans. Microb Ecol 58: 737-752.
61. Pham VD, Konstantinidis KT, Palden T & DeLong EF (2008) Phylogenetic analyses of ribosomal DNA-containing bacterioplankton genome fragments from a 4000 m vertical profile in the North Pacific Subtropical Gyre. Environ Microbiol 10: 2313-2330.
62. Pruesse L, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J & Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
63. Reeburgh WS & Heggie DT (1977) Microbial methane consumption reactions and their effect on methane distributions in freshwater and marine environment. Limnol Oceanogr 22: 1-9.
64. Reichenbach H, Lang E, Schumann P & Sproer C (2006) Byssovorax cruenta gen. nov., sp. nov., nom. rev., a cellulose-degrading myxobacterium: rediscovery of 'Myxococcus cruentus' Thaxter 1897. Int J Syst Bacteriol 56: 2357-2363.
65. Reysenbach AL & Pace N (1995) Reliable amplification of hyperthemophilic archaeal 16S rRNA genes by PCR. Thermophiles ( Robb F & Place A, eds), pp. 101-106. Cold Spring Habor Press, Cold Spring Harbor, NY.
66. Schleper C, Jurgens G & Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3: 479-488.
67. Schloss PD, Westcott SL, Ryabin T et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
68. Senior E, Lindstrom EB, Banat IM & Nedwell DB (1982) Sulfate reduction and methanogenesis in the sediment of a saltmarsh on the east coast of the United Kingdom. Appl Environ Microbiol 43: 987-996.
69. Shimkets L, Dworkin M & Reichenbach H (2006) The Myxobacteria. The Prokaryotes ( Dworkin M, Falkow S, Rosenberg E, Schleifer K-H & Stackebrandt E, eds), pp. 31-115. Springer, New York.
70. Smith CR & Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanography and Marine Biology, Vol. 41 ( Gibson RN & Atkinson RJA, eds), pp. 311-354. CRC Press, Boca Raton, FL.
71. Takai K & Horikoshi K (1999) Genetic diversity of Archaea in deep-sea hydrothermal vent environments. Genetics 152: 1285-1297.
72. Taylor CD, Wirsen CO & Gaill F (1999) Rapid microbial production of filamentous sulfur mats at hydrothermal vents. Appl Environ Microbiol 65: 2253-2255.
73. Teske A & Sorensen KB (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J 2: 3-18.
74. Teske A, Hinrichs K-U, Edgcomb V, de Vera Gomez A, Kysela D, Sylva SP, Sogin ML & Jannasch HW (2002) Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Appl Environ Microbiol 68: 1994-2007.
75. Thompson JR, Marcelino LA & Polz MF (2002) Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by 'reconditioning PCR'. Nucleic Acids Res 30: 2083-2088.
76. Vetriani C, Jannasch HW, MacGregor BJ, Stahl DA & Reysenbach AL (1999) Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl Environ Microbiol 65: 4375-4384.
77. Webb CO, Ackerly DD, McPeek MA & Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33: 475-505.
78. Webb CO, Ackerly DD & Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24: 2098-2100.
79. Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21: 213-251.
80. Winfrey MR & Zeikus JG (1977) Effect of sulfate on carbon and electron flow during microbial methanogenesis in freshwater sediments. Appl Environ Microbiol 33: 275-281.
81. Wirsen CO, Sievert SM, Cavanaugh CM, Molyneaux SJ, Ahmad A, Taylor LT, DeLong EF & Taylor CD (2002) Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur. Appl Environ Microbiol 68: 316-325.
82. Wolff T (1979) Macrofaunal utilization of plant remains in the deep sea. Sarsia 64: 117-136.