Seagrass (Zostera marina) colonization promotes the accumulation of diazotrophic bacteria and alters the relative abundances of specific bacterial lineages involved in benthic carbon and sulfur cycling

Applied and Environmental Microbiology

Volumn 81, Issue 19, 2015, Pages 6901-6914

  Sun, Feifei ^a,b,c   Zhang, Xiaoli ^b   Zhang, Qianqian ^b   Liu, Fanghua ^b   Zhang, Jianping ^a,c   Gong, Jun ^b  

^a JIANGSU UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b YANTAI INSTITUTE OF COASTAL ZONE RESEARCH   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOCHEMISTRY; BIOGEOCHEMISTRY; CARBON; ECOLOGY; GENES; NITROGEN; PLANTS (BOTANY); POPULATION STATISTICS; RNA; SEDIMENTS; SULFUR;

BACTERIAL COMMUNITY STRUCTURE; CARBON-TO-NITROGEN RATIO; DIAZOTROPHIC BACTERIA; HIGH-THROUGHPUT SEQUENCING; NITROGENASE GENES (NIFH); PHYLOGENETIC ANALYSIS; SEDIMENTARY ENVIRONMENT; TERMINAL RESTRICTION FRAGMENT LENGTH POLYMORPHISMS;

ORGANIC CARBON;

BACTERIUM; BENTHIC ENVIRONMENT; BIOACCUMULATION; BIOAVAILABILITY; BIOGEOCHEMISTRY; CARBON CYCLE; COASTAL LAGOON; COLONIZATION; COMMUNITY STRUCTURE; CONCENTRATION (COMPOSITION); GENE EXPRESSION; GENOTYPE; RELATIVE ABUNDANCE; SEAGRASS; SULFUR CYCLE;

CHINA;

ANAEROLINEAE; BACTERIA (MICROORGANISMS); BACTEROIDETES; CHLOROFLEXI; CHLOROFLEXI (CLASS); DELTAPROTEOBACTERIA; DESULFOBULBACEAE; DESULFOBULBUS; DESULFOCAPSA; DESULFOCOCCUS; FLAVOBACTERIACEAE; GEOBACTERACEAE; PSEUDOMONAS; ZOSTERA MARINA;

CARBON; NITROGEN; SULFUR;

BACTERIUM; BIODIVERSITY; CHINA; CLASSIFICATION; ECOSYSTEM; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NITROGEN FIXATION; PHYLOGENY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SEDIMENT; ZOSTERACEAE;

BACTERIA; BIODIVERSITY; CARBON; CHINA; ECOSYSTEM; GEOLOGIC SEDIMENTS; MOLECULAR SEQUENCE DATA; NITROGEN; NITROGEN FIXATION; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SULFUR; ZOSTERACEAE;

EID: 84940750121     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01382-15     Document Type: Article

References (78)

1. Duarte CM, Holmer M, Marbh N. 2005. Plant-microbe interactions in seagrass meadows, p 31-59. In Kristensen E, Haese RR, Kostka JE (ed), Interactions between macro-and microorganisms in marine sediments. Coastal and estuarine studies, vol 60. American Geophysical Union, New York, NY.
2. Caffrey JM, Kemp WM. 1990. Nitrogen cycling in sediments with estuarine populations of Potamogeton perfoliatus and Zostera marina. Mar Ecol Prog Ser 66:147-160. http://dx.doi.org/10.3354/meps066147.
3. Miyajima T, Koike I, Yamano H, Iizumi H. 1998. Accumulation and transport of seagrass-derived organic matter in reef flat sediment of Green Island, Great Barrier Reef. Mar Ecol Prog Ser 175:251-259. http://dx.doi.org/10.3354/meps175251.
4. Devereux R. 2005. Seagrass rhizosphere microbial communities, p 199-216. In Kristensen E, Haese RR, Kostka JE (ed), Interactions between macro-and microorganisms in marine sediments. Coastal and estuarine studies, vol 60. American Geophysical Union, New York, NY.
5. Moriarity DJW, Iverson RI, Pollard PC. 1986. Exudation of organic carbon by the seagrass Halodule wrightii Aschers, and its effect on bacterial growth in the sediment. J Exp Mar Biol Ecol 96:115-126. http://dx.doi.org/10.1016/0022-0981(86)90237-6.
6. Holmer M, Andersen FØ, Nilesen SL, Boschker HTS. 2001. The importance of mineralization based on sulfate reduction for nutrient regeneration in tropical seagrass sediments. Aquat Bot 71:1-17. http://dx.doi.org/10.1016/S0304-3770(01)00170-X.
7. Smith AC, Kostka JE, Devereux R, Yates DF. 2004. Seasonal composition and activity of sulfate reducing prokaryotic communities in seagrass bed sediment. Aquat Microb Ecol 37:183-195. http://dx.doi.org/10.3354/ame037183.
8. Küsel K, Trinkwalter T, Drake HL, Devereux R. 2006. Comparative evaluation of anaerobic bacterial communities associated with roots of submerged macrophytes growing in marine or brackish water sediments. J Exp Mar Biol Ecol 337:49-58. http://dx.doi.org/10.1016/j.jembe.2006.06.004.
9. Welsh DT. 2000. Nitrogen fixation in seagrass meadows: regulation, plant-bacteria interactions and significance to primary productivity. Ecol Lett 3:58-71. http://dx.doi.org/10.1046/j.1461-0248.2000.00111.x.
10. Capone DG, Budin JM. 1982. Nitrogen-fixation associated with rinsed roots and rhizomes of the eelgrass Zostera marina. Plant Physiol 70:1601-1604. http://dx.doi.org/10.1104/pp.70.6.1601.
11. Nielsen LB, Finster K, Welsh DT, Donelly A, Herbert RA, De Wit R, Lomstein BA. 2001. Sulphate reduction and nitrogen fixation rates associated with roots, rhizomes and sediments from Zostera noltii and Spartina maritima meadows. Environ Microbiol 3:63-71. http://dx.doi.org/10.1046/j.1462-2920.2001.00160.x.
12. Shieh WY, Simidu U, Maruyama Y. 1989. Enumeration and characterization of nitrogen-fixing bacteria in an eelgrass (Zostera marina) bed. Microb Ecol 18:249-259. http://dx.doi.org/10.1007/BF02075812.
13. Raja S, Thangaradjou T, Sivakumar K, Kannan L. 2012. Rhizobacterial population density and nitrogen fixation in seagrass community of Gulf of Mannar, India. J Environ Biol 33:1033-1037.
14. Lovell CR, Piceno YM, Quattro JM, Bagwell CE. 2000. Molecular analysis of diazotroph diversity in the rhizosphere of the smooth cordgrass, Spartina alterniflora. Appl Environ Microbiol 66:3814-3822. http://dx.doi.org/10.1128/AEM.66.9.3814-3822.2000.
15. Bagwell CE, La Rocque JR, Smith GW, Polson SW, Friez MJ, Longshore JW, Lovell CR. 2002. Molecular diversity of diazotrophs in oligotrophic tropical seagrass bed communities. FEMS Microbiol Ecol 39:113-119. http://dx.doi.org/10.1111/j.1574-6941.2002.tb00912.x.
16. Thamdrup B. 2000. Bacterial manganese and iron reduction in aquatic sediments. Adv Microb Ecol 16:41-84. http://dx.doi.org/10.1007/978-1-4615-4187-5_2.
17. Marbà N, Holmer M, Gacia E, Barrón C. 2006. Seagrass beds and coastal biogeochemistry, p 135-157. In Larkum AWD, Orth RJ, Duarte CM (ed), Seagrasses: biology, ecology and conservation. Springer, Amsterdam, Netherlands.
18. Cifuentes A, Antón J, Benlloch S, Donnelly A, Herbert RA, Rodrígues-Valera F. 2000. Prokaryotic diversity in Zostera noltii-colonized marine sediments. Appl Environ Microbiol 66:1715-1719. http://dx.doi.org/10.1128/AEM.66.4.1715-1719.2000.
19. Jensen SI, Kühl M, Priemé A. 2007. Different bacterial communities associated with the roots and bulk sediment of the seagrass Zostera marina. FEMS Microbiol Ecol 62:108-117. http://dx.doi.org/10.1111/j.1574-6941.2007.00373.x.
20. James JB, Sherman TD, Devereux R. 2006. Analysis of bacterial communities in seagrass bed sediments by double-gradient denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA genes. Microb Ecol 52: 655-661. http://dx.doi.org/10.1007/s00248-006-9075-3.
21. Zhang X, Song Y, Liu D, Keesing JK, Gong J. 18 December 2014. Macroalgal blooms favor heterotrophic diazotrophic bacteria in nitrogenrich and phosphorus-limited coastal surface waters in the Yellow Sea. Estuar Coast Shelf Sci http://dx.doi.org/10.1016/j.ecss.2014.12.015.
22. Zhang X, Agogué H, Dupuy C, Gong J. 2014. Relative abundance of ammonia oxidizers, denitrifiers, and anammox bacteria in sediments of hyper-nutrified estuarine tidal flats and in relation to environmental conditions. Clean Soil Air Water 42:815-823. http://dx.doi.org/10.1002/clen.201300013.
23. Poly F, Monrozier LJ, Bally R. 2001. Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95-103. http://dx.doi.org/10.1016/S0923-2508(00)01172-4.
24. Zehr JP, Jenkins BD, Short SM, Steward GF. 2003. Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539-554. http://dx.doi.org/10.1046/j.1462-2920.2003.00451.x.
25. Raymond J, Siefert JL, Staples CR, Blankenship RE. 2004. The natural history of nitrogen fixation. Mol Biol Evol 21:541-554.
26. Kechris KJ, Lin JC, Bickel PJ, Glazer AN. 2006. Quantitative exploration of the occurrence of lateral gene transfer by using nitrogen fixation genes as a case study. Proc Natl Acad Sci USA 103:9584-9589. http://dx.doi.org/10.1073/pnas.0603534103.
27. Muyzer G, De Waal EC, Uitterlinden AG. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695-700.
28. Caporaso JG, Kuczynki J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
29. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. http://dx.doi.org/10.1093/bioinformatics/btq461.
30. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610-618. http://dx.doi.org/10.1038/ismej.2011.139.
31. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. 2010. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266-267. http://dx.doi.org/10.1093/bioinformatics/btp636.
32. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methé B, DeSantis TZ, The Human Microbiome Consortium, Petrosino JF, Knight R, Birren BW. 2011. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494-504. http://dx.doi.org/10.1101/gr.112730.110.
33. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98.
34. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09.
35. Dang H, Luan X, Zhao J, Li J. 2009. Diverse and novel nifH and nifH-like gene sequences in the deep-sea methane seep sediments of the Okhotsk Sea. Appl Environ Microbiol 75:2238-2245. http://dx.doi.org/10.1128/AEM.02556-08.
36. Good IJ. 1953. The population frequencies of species and the estimation of population parameters. Biometrika 40:237-264.
37. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680. http://dx.doi.org/10.1093/nar/22.22.4673.
38. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313. http://dx.doi.org/10.1093/bioinformatics/btu033.
39. Darriba D, Taboada GL, Doallo R, Posada D. 2011. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164-1165. http://dx.doi.org/10.1093/bioinformatics/btr088.
40. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729. http://dx.doi.org/10.1093/molbev/mst197.
41. Hamady M, Lozupone C, Knight R. 2010. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17-27. http://dx.doi.org/10.1038/ismej.2009.97.
42. ter Braak CJF, Smilauer P. 2002. CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, NY.
43. Fulweiler RW, Brown SM, Nixon SW, Jenkins BD. 2013. Evidence and a conceptual model for the co-occurrence of nitrogen fixation and denitrification in heterotrophic marine sediments. Mar Ecol Prog Ser 482:57-68. http://dx.doi.org/10.3354/meps10240.
44. Brown SM, Jenkins BD. 2014. Profiling gene expression to distinguish the likely active diazotrophs from a sea of genetic potential in marine sediments. Environ Microbiol 16:3128-3142. http://dx.doi.org/10.1111/1462-2920.12403.
45. Pfeffer C, Larsen S, Song J, Dong M, Besenbacher F, Meyer RL, Kjeldsen KU, Schreiber L, Gorby YA, El-Naggar MY, Leung KM, Schramm A, Risgaard-Petersen N, Nielsen LP. 2012. Filamentous bacteria transport electrons over centimetre distances. Nature 491:218-221. http://dx.doi.org/10.1038/nature11586.
46. Welsh DT, Bourgues S, de Wit R, Herbert RA. 1996. Seasonal variations in nitrogen-fixation (acetylene reduction) and sulphate-reduction rates in the rhizosphere of Zostera noltii: nitrogen fixation by sulphate-reducing bacteria. Mar Biol 125:619-628. http://dx.doi.org/10.1007/BF00349243.
47. Gacia E, Duane CM. 2001. Sediment retention by a Mediterranean Posidonia oceanica meadow: the balance between deposition and resuspension. Estuar Coast Shelf Sci 52:505-514. http://dx.doi.org/10.1006/ecss.2000.0753.
48. Maslennikova S, Larina N, Larin S. 2012. The effect of sediment grain size on heavy metal content. Lakes Reserv Ponds 6:43-54.
49. Gong J, Shi F, Ma B, Dong J, Pachiadaki M, Zhang X, Edgcomb VP. 11 January 2015. Depth shapes α-and β-diversities of microbial eukaryotes in surficial sediments of coastal ecosystems. Environ Microbiol http://dx.doi.org/10.1111/1462-2920.12763.
50. Bauer K, Díez B, Lugomela C, Seppälä S, Borg AJ, Bergman B. 2008. Variability in benthic diazotrophy and cyanobacterial diversity in a tropical intertidal lagoon. FEMS Microbiol Ecol 63:205-221. http://dx.doi.org/10.1111/j.1574-6941.2007.00423.x.
51. Gaby JC, Buckley DH. 2012. A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLoS One 7:e42149. http://dx.doi.org/10.1371/journal.pone.0042149.
52. Donnelly AP, Herbert RA. 1999. Bacterial interactions in the rhizosphere of seagrass communities in shallow coastal lagoons. J Appl Microbiol Symp Suppl 85:151S-160S.
53. Dias ACF, Pereirae Silva MC, Cotta SR, Dini-Andreote F, Soares FL, Salles JF, Azevedo JL, van Elsas JD, Andreote FD. 2012. Abundance and genetic diversity of nifH gene sequences in anthropogenically affected Brazilian mangrove sediments. Appl Environ Microbiol 78:7960-7967. http://dx.doi.org/10.1128/AEM.02273-12.
54. Bernard RJ, Mortazavi B, Wang L, Ortmann AC, MacIntyre H, Burnett WC. 2014. Benthic nutrient fluxes and limited denitrification in a subtropical groundwater-influenced coastal lagoon. Mar Ecol Prog Ser 504: 13-26. http://dx.doi.org/10.3354/meps10783.
55. Dang H, Yang J, Li J, Luan X, Zhang Y, Gu G, Xue R, Zong M, Klotz MG. 2013. Environment-dependent distribution of the sediment nifHharboring microbiota in the northern South China Sea. Appl Environ Microbiol 79:121-132. http://dx.doi.org/10.1128/AEM.01889-12.
56. Holmes DE, Finneran KT, O'Neil RA, Lovley DR. 2002. Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer sediments. Appl Environ Microbiol 68:2300-2306. http://dx.doi.org/10.1128/AEM.68.5.2300-2306.2002.
57. Holmes DE, Nicoll JS, Bond DR, Lovley DR. 2004. Potential role of a novel psychrotolerant member of the family Geobacteraceae, Geopsychrobacter electrodiphilus gen. nov., sp. nov., in electricity production by a marine sediment fuel cell. Appl Environ Microbiol 70:6023-6030. http://dx.doi.org/10.1128/AEM.70.10.6023-6030.2004.
58. Sass A, Rütters H, Cypionka H, Sass H. 2002. Desulfobulbus mediterraneus sp. nov., a sulfate-reducing bacterium growing on mono-and disaccharides. Arch Microbiol 177:468-474. http://dx.doi.org/10.1007/s00203-002-0415-5.
59. Finster K, Liesack W, Thamdrup B. 1998. Elemental sulfur and thiosulfate disproportionation by Desulfocapsa sulfoexigens sp. nov., a new anaerobic bacterium isolated from marine surface sediment. Appl Environ Microbiol 64:119-125.
60. Finster KW, Kjeldsen KU, Kube M, Reinhardt R, Mussmann M, Amann R, Schreiber L. 2013. Complete genome sequence of Desulfocapsa sulfexigens, a marine deltaproteobacterium specialized in disproportionating inorganic sulfur compounds. Stand Genomic Sci 8:58-68. http://dx.doi.org/10.4056/sigs.3777412.
61. Muehe EM, Gerhardt S, Schink B, Kappler A. 2009. Ecophysiology and the energetic benefit of mixotrophic Fe(II) oxidation by various strains of nitrate-reducing bacteria. FEMS Microbiol Ecol 70:335-343. http://dx.doi.org/10.1111/j.1574-6941.2009.00755.x.
62. Podgorsek L, Imhoff JF. 1999. Tetrathionate production by sulfur oxidizing bacteria and the role of tetrathionate in the sulfur cycle of Baltic Sea sediments. Aquat Microb Ecol 17:255-265. http://dx.doi.org/10.3354/ame017255.
63. Bertics VJ, Sohm JA, Treude T, Chow CET, Capone DG, Fuhrman JA, Ziebis W. 2010. Burrowing deeper into benthic nitrogen cycling: the impact of bioturbation on nitrogen fixation coupled to sulfate reduction. Mar Ecol Prog Ser 409:1-15. http://dx.doi.org/10.3354/meps08639.
64. Rosado AS, Duarte GF, Seldin L, van Elsas JD. 1998. Genetic diversity of nifH gene sequences in Paenibacillus azotofixans strains and soil samples analyzed by denaturing gradient gel electrophoresis of PCR-amplified gene fragments. Appl Environ Microbiol 64:2770-2779.
65. Poly F, Ranjard L, Nazaret S, Gourbère F, Monrozier LJ. 2001. Comparison of nifH gene pools in soils and soil microenvironments with contrasting properties. Appl Environ Microbiol 67:2255-2262. http://dx.doi.org/10.1128/AEM.67.5.2255-2262.2001.
66. Loka Bharathi PA, Sathe V, Chandramohan D. 1990. Effect of lead, mercury and cadmium on a sulphate-reducing bacterium. Environ Pollut 67:361-374. http://dx.doi.org/10.1016/0269-7491(90)90072-K.
67. Singh S, Shrivastava AK, Singh VK. 2014. Arsenic and cadmium are inhibitors of cyanobacterial dinitrogenase reductase (nifH1) gene. Funct Integr Genomics 14:571-580. http://dx.doi.org/10.1007/s10142-014-0375-2.
68. Kenworthy WJ, Thayer GW. 1984. Production and decomposition of the roots and rhizomes of seagrasses, Zostera marina and Thalassia testudinum, in temperate and subtropical marine ecosystems. Bull Mar Sci 35: 364-379.
69. Meyers PA. 1994. Preservation of elemental and isotopic source identification of sedimentary organic matter. Chem Geol 114:289-302. http://dx.doi.org/10.1016/0009-2541(94)90059-0.
70. Widdel F, Bak F. 1992. Gram-negative mesophilic sulfate-reducing bacteria, p 3352-3378. In Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (ed), The prokaryotes, 2nd ed, vol 1. Springer-Verlag, New York, NY.
71. Kniemeyer O, Musat F, Sievert SM, Knittel K, Wilkes H, Blumenberg M, Michaelis W, Classen A, Bolm C, Joye SB, Widdel F. 2007. Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449:898-902. http://dx.doi.org/10.1038/nature06200.
72. Ravenschlag K, Sahm K, Knoblauch C, Jørgensen BB, Amann R. 2000. Community structure, cellular rRNA content, and activity of sulfatereducing bacteria in marine Arctic sediments. Appl Environ Microbiol 66:3592-3602. http://dx.doi.org/10.1128/AEM.66.8.3592-3602.2000.
73. Llobet-Brossa E, Rabus R, Böttcher ME, Könneke M, Finke N, Schramm A, Meyer RL, Grötzschel S, Rosselló-Mora R, Amann R. 2002. Community structure and activity of sulfate-reducing bacteria in an intertidal surface sediment: a multi-method approach. Aquat Microb Ecol 29: 211-226. http://dx.doi.org/10.3354/ame029211.
74. Kleindienst S, Ramette A, Amann R, Knittel K. 2012. Distribution and in situ abundance of sulfate-reducing bacteria in diverse marine hydrocarbon seep sediments. Environ Microbiol 14:2689-2710. http://dx.doi.org/10.1111/j.1462-2920.2012.02832.x.
75. Kirchman DL. 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91-100. http://dx.doi.org/10.1111/j.1574-6941.2002.tb00910.x.
76. Yamada T, Sekiguchi Y. 2009. Cultivation of uncultured Chloroflexi subphyla: significance and ecophysiology of formerly uncultured Chloroflexi 'subphylum I' with natural and biotechnological relevance. Microbes Environ 24:205-216. http://dx.doi.org/10.1264/jsme2.ME09151S.
77. Hug LA, Castelle CJ, Wrighton KC, Thomas BC, Sharon I, Frischkorn KR, Williams KH, Tringe SG, Banfield JF. 2013. Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome 1:22. http://dx.doi.org/10.1186/2049-2618-1-22.
78. Cabezas A, Pommerenke B, Boon N, Friedrich MW. 2015. Geobacter, Anaeromyxobacter and Anaerolineae populations are enriched on anodes of root exudate-driven microbial fuel cells in rice field soil. Environ Microbiol Rep 7:489-497. http://dx.doi.org/10.1111/1758-2229.12277.