Complex coupled metabolic and prokaryotic community responses to increasing temperatures in anaerobic marine sediments: Critical temperatures and substrate changes

FEMS Microbiology Ecology

Volumn 91, Issue 8, 2015, Pages

  Roussel, Erwan G ^a   Cragg, Barry A ^a   Webster, Gordon ^a,b   Sass, Henrik ^a   Tang, Xiaohong ^a   Williams, Angharad S ^b   Gorra, Roberta ^c   Weightman, Andrew J ^b   Parkes, R John ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

Acetogenesis; Anaerobic processes; Chemolithotrophic; Chemoorganotrophic; Methanogenesis; Mineralisation; Sediment; Sulphate reduction; Temperature

Indexed keywords

ANOXIC CONDITIONS; BIOMINERALIZATION; CHEMOAUTOTROPHY; COMMUNITY RESPONSE; MARINE SEDIMENT; METABOLISM; METHANOTROPHY; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; PROKARYOTE; REDUCTION; SULFATE; SULFATE-REDUCING BACTERIUM; TEMPERATURE EFFECT;

ARCHAEA; BACTERIA (MICROORGANISMS); EURYARCHAEOTA; PROKARYOTA;

METHANE; RNA 16S; SULFATE;

ANAEROBIC GROWTH; BACTERIUM; CHEMOAUTOTROPHY; EURYARCHAEOTA; EUTROPHICATION; GENETICS; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHYLOGENY; PHYSIOLOGY; SEDIMENT; TEMPERATURE;

ANAEROBIOSIS; BACTERIA; CHEMOAUTOTROPHIC GROWTH; EURYARCHAEOTA; EUTROPHICATION; GEOLOGIC SEDIMENTS; METHANE; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SULFATES; TEMPERATURE;

EID: 84949235764     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec/fiv084     Document Type: Article

References (88)

1. Aller RC, Yingst JY. Relationships between microbial distributions and the anaerobic decomposition of organic-matter in surface sediments of long-island sound, USA. Mar Biol 1980;56:29-42.
2. Altschul SF, Gish W, MillerW, et al. Basic local alignment search tool. J Mol Biol 1990;215:403-10.
3. Arnosti C. Speed bumps and barricades in the carbon cycle: substrate structural effects on carbon cycling. Mar Chem 2004;92:263-73.
4. Aullo T, Ranchou-Peyruse A, Ollivier B, et al. Desulfotomaculum spp. and related Gram-positive sulfate-reducing bacteria in deep subsurface environments. Front Microbiol 2013; 4:362.
5. Biddle JF, Cardman Z, Mendlovitz H, et al. Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sediments. ISME J 2012;6:1018-31.
6. Biddle JF, Lipp JS, Lever MA, et al. Heterotrophic Archaea dominate sedimentary subsurface ecosystems offPeru. P Natl Acad Sci USA 2006;103:3846-51.
7. Bragg L, Stone G, Imelfort M, et al. Fast, accurate errorcorrection of amplicon pyrosequences using Acacia. Nat Methods 2012;9:425-6.
8. Burdige DJ. Temperature dependence of organic matter remineralization in deeply-buried marine sediments. Earth Planet Sc Lett 2011;311:396-410.
9. Canfield DE, Jørgensen BB, Fossing H, et al. Pathways of organiccarbon oxidation in three continental-margin sediments. Mar Geol 1993;113:27-40.
10. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-6.
11. Conrad R, Klose M, Noll M. Functional and structural response of the methanogenic microbial community in rice field soil to temperature change. Environ Microbiol 2009;11: 1844-53.
12. Conrad R, Wetter B. Influence of temperature on energetics of hydrogen metabolism in homoacetogenic, methanogenic, and other anaerobic bacteria. Arch Microbiol 1990;155: 94-8.
13. de Rezende JR, Kjeldsen KU, Hubert CRJ, et al. Dispersal of thermophilic Desulfotomaculum endospores into Baltic Sea sediments over thousands of years. ISME J 2013;7:72-84.
14. Delong EF. Archaea in coastal marine environments. PNatl Acad Sci USA 1992;89:5685-9.
15. DeSantis TZ, Hugenholtz P, Larsen N, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microb 2006;72:5069-72.
16. Dolfing J, Larter SR, Head IM. Thermodynamic constraints on methanogenic crude oil biodegradation. ISME J 2008;2: 442-52.
17. Dridi B, Fardeau ML, Ollivier B, et al. Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Micr 2012;62:1902-7.
18. Edgar RC. Search and clustering orders ofmagnitude faster than BLAST. Bioinformatics 2010;26:2460-1.
19. Fardeau ML, Magot M, Patel BKC, et al. Thermoanaerobacter subterraneus sp nov., a novel thermophile isolated from oilfield water. Int J Syst Evol Micr 2000;50:2141-9.
20. Fey A, Conrad R. Effect of temperature on carbon and electron flow and on the archaeal community in methanogenic rice field soil. Appl Environ Microb 2000;66:4790-7.
21. Finke N, Hoehler T, Jørgensen B. Hydrogen 'leakage' during methanogenesis from methanol and methylamine: implications for anaerobic carbon degradation pathways in aquatic sediments. Environ Microbiol 2007;9:1060-71.
22. Finke N, Jørgensen BB. Response of fermentation and sulfate reduction to experimental temperature changes in temperate and Arctic marine sediments. ISME J 2008;2:815-29.
23. Finke N, Vandieken V, Jørgensen BB. Acetate, lactate, propionate, and isobutyrate as electron donors for iron and sulfate reduction in Arctic marine sediments, Svalbard. FEMS Microbiol Ecol 2007;59:10-22.
24. Fry JC, Parkes RJ, Cragg BA, et al. Prokaryotic biodiversity and activity in the deep subseafloor biosphere. FEMS Microbiol Ecol 2008;66:181-96.
25. Hedges JI, Keil RG. Marine Chemistry Discussion Paper. Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar Chem 1995;4:81-115.
26. Ho DP, Jensen PD, Batstone DJ. Methanosarcinaceae and acetateoxidizing pathways dominate in high-rate thermophilic anaerobic digestion of waste-activated sludge. Appl Environ Microb 2013;79:6491-500.
27. Holler T, Widdel F, Knittel K, et al. Thermophilic anaerobic oxidation of methane by marine microbial consortia. ISME J 2011;5:1946-56.
28. Horsfield B, Schenk HJ, Zink K, et al. Living microbial ecosystems within the active zone of catagenesis: implications for feeding the deep biosphere. Earth Planet Sci Lett 2006;246:55-69.
29. Hubert C, Arnosti C, Bruchert V, et al. Thermophilic anaerobes in Arctic marine sediments induced to mineralize complex organic matter at high temperature. Environ Microbiol 2010;12:1089-104.
30. Hubert C, Loy A, Nickel M, et al. A constant flux of diverse thermophilic Bacteria into the cold Arctic seabed. Science 2009;325:1541-4.
31. Isaksen MF, Bak F, Jørgensen BB. Thermophilic sulfate-reducing bacteria in cold marine sediments. FEMS Microbiol Ecol 1994;14:1-8.
32. Jiang L, Long C, Wu X, et al. Optimization of thermophilic fermentative hydrogen production by the newly isolated Caloranaerobacter azorensis H53214 from deep-sea hydrothermal vent environment. Int J Hydrogen Energ 2014;39: 14154-60.
33. Jørgensen BB. Mineralization of organic-matter in the sea bed- the role of sulfate reduction. Nature 1982;296:643-5.
34. Jørgensen BB. Processes at the sediment-water interface. In: Bolin B, Cook RB (eds) TheMajor Biogeochemical Cycles and Their Interactions. New York: Wiley, 1983, 477-509.
35. Joyce AE. The coastal temperature network and ferry route programme: long-term temperature and salinity observations. CEFAS Sci Ser 2006;43:1-129.
36. Kallmeyer J, Boetius A. Effects of temperature and pressure on sulfate reduction and anaerobic oxidation of methane in hydrothermal sediments of Guaymas Basin. Appl Environ Microbiol 2004;70:1231-3.
37. Koga Y. Thermal adaptation of the Archaeal and Bacterial lipid membranes. Archaea 2012;2012:789652.
38. Kotelnikova S, Pedersen K. Evidence for methanogenic Archaea and homoacetogenic Bacteria in deep granitic rock aquifers. FEMS Microbiol Rev 1997;20:339-49.
39. Kryachko Y, Dong XL, Sensen CW, et al. Compositions of microbial communities associated with oil and water in a mesothermic oil field. Anton Leeuw 2012;101:493-506.
40. Lipp JS, Morono Y, Inagaki F, et al. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 2008;454:991-4.
41. Lloyd KG, Schreiber L, Petersen DG, et al. Predominant archaea in marine sediments degrade detrital proteins. Nature 2013;496:215-8.
42. Lovley DR, Chapelle FH. Deep subsurface microbial processes. Rev Geophys 1995;33:365-81.
43. Mayumi D, Dolfing J, Sakata S, et al. Carbon dioxide concentration dictates alternative methanogenic pathways in oil reservoirs. Nat Commun 2013;4:1998.
44. Mayumi D, Mochimaru H, Yoshioka H, et al. Evidence for syntrophic acetate oxidation coupled to hydrogenotrophic methanogenesis in the high-temperature petroleum reservoir of Yabase oil field Japan. Environ Microbiol 2011;13:1995-2006.
45. Meng J, Xu J, Qin D, et al. Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses. ISME J 2014;8:650-9.
46. Middelburg JJ, Klaver G, Nieuwenhuize J, et al. Organic matter mineralization in intertidal sediments along an estuarine gradient. Mar Ecol-Prog Ser 1996;132:157-68.
47. Mikucki JA, Liu YT, Delwiche M, et al. Isolation of a methanogen from deep marine sediments that contain methane hydrates, and description of Methanoculleus submarinus sp. nov. Appl Environ Microb 2003;69:3311-6.
48. Moreno T, Oldroyd A, McDonald I, et al. Preferential fractionation of trace metals-metalloids into PM10 resuspended from contaminated goldmine tailings at Rodalquilar, Spain. Water Air Soil Poll 2007;179:93-105.
49. Muller AL, de Rezende JR, Hubert CRJ et al. Endospores of thermophilic bacteria as tracers of microbial dispersal by ocean currents. ISME J 2014;86:1153-65.
50. Mussmann M, Brito I, Pitcher A, et al. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. P Natl Acad Sci USA 2011;108:16771-6.
51. Muyzer G, BrinkoffT, Nübel U, et al. Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Akkermans ADL, Van Elsas JD, De Bruijn FJ, et al. (eds). Molecular Microbial Ecology Manual. Dordrecht: Kluwer Academic Publishers, 1998, 1-27.
52. Muyzer G, Dewaal EC, Uitterlinden AG. Profiling of complex microbial-populations by denaturing gradient gelelectrophoresis analysis of polymerase chain reactionamplified genes-coding for 16S rRNA. Appl Environ Microbiol 1993;59:695-700.
53. Nozhevnikova AN, Nekrasova V, Ammann A, et al. Influence of temperature and high acetate concentrations on methanogenensis in lake sediment slurries. FEMS Microbiol Ecol 2007;62:336-44.
54. O'Sullivan LA, Roussel EG, Weightman AJ, et al. Survival of Desulfotomaculum spores from estuarine sediments after serial autoclaving and high-temperature exposure. ISME J 2015;9:922-33.
55. O'Sullivan LA, Sass AM, Webster G, et al. Contrasting relationships between biogeochemistry and prokaryotic diversity depth profiles along an estuarine sediment gradient. FEMS Microbiol Ecol 2013;85:143-57.
56. O'Sullivan LA, Webster G, Fry JC, et al. Modified linker-PCR primers facilitate complete sequencing of DGGE DNA fragments. J Microbiol Meth 2008;75:579-81.
57. Oremland RS, Marsh LM, Polcin S. Methane production and simultaneous sulphate reduction in anoxic, salt marsh sediments. Nature 1982;296:143-5.
58. Ovreas L, Forney L, Daae FL, et al. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 1997;63:3367-73.
59. Parkes RJ, Brock F, Banning N, et al. Changes in methanogenic substrate utilization and communities with depth in a saltmarsh, creek sediment in southern England. Estuar Coast Shelf S 2012;96:170-8.
60. Parkes RJ, Cragg B, Roussel E, et al. A review of prokaryotic populations and processes in sub-seafloor sediments, including biosphere:geosphere interactions. Mar Geol 2014;352: 409-25.
61. Parkes RJ, Cragg BA, Banning N, et al. Biogeochemistry and biodiversity of methane cycling in subsurface marine sediments Skagerrak, Denmark. Environ Microbiol 2007a;9: 1146-61.
62. Parkes RJ, Gibson GR, Mueller-Harvey I, et al. Determination of the substrates for sulfate-reducing bacteria within marine and estuarine sediments with different rates of sulfate reduction. J Gen Microbiol 1989;135:175-87.
63. Parkes RJ, Wellsbury P, Mather ID, et al. Temperature activation of organic matter and minerals during burial has the potential to sustain the deep biosphere over geological time scales. Org Geochem 2007b;38:845-52.
64. Paul K, Nonoh JO, Mikulski L, et al. 'Methanoplasmatales,' Thermoplasmatales-related Archaea in termite guts and other environments, are the seventh order of methanogens. Appl Environ Microbiol 2012;78:8245-53.
65. Peters V, Conrad R. Sequential reduction processes and initiation of CH4 poduction upon flooding of oxic upland soils. Soil Biol Biochem 1996;28:371-82.
66. Rinke C, Schwientek P, Sczyrba A, et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 2013;499:431-7.
67. Robador A, Bruchert V, Jørgensen BB. The impact of temperature change on the activity and community composition of sulfate-reducing bacteria in arctic versus temperate marine sediments. Environ Microbiol 2009;11:1692-703.
68. Roh Y, Liu SV, Li GS, et al. Isolation and characterization of metalreducing Thermoanaerobacter strains from deep subsurface environments of the Piceance Basin, Colorado. Appl Environ Microbiol 2002;68:6013-20.
69. Rothfuss F, Conrad R. Thermodynamics of methanogenic intermediary metabolism in littoral sediment of Lake Constance. FEMS Microbiol Ecol 1993;12:265-76.
70. Roussel EG, Cambon-Bonavita MA, Querellou J, et al. Extending the sub-sea-floor biosphere. Science 2008;320:1046.
71. Rui J, Qiu Q, Lu Y. Syntrophic acetate oxidation under thermophilic methanogenic condition in Chinese paddy field soil. FEMS Microbiol Ecol 2011;77:264-73.
72. Schouten S, Middelburg JJ, Hopmans EC, et al. Fossilization and degradation of intact polar lipids in deep subsurface sediments: a theoretical approach. Geochim Cosmochim Acta 2010;74:3806-14.
73. Seewald JS. Organic-inorganic interactions in petroleumproducing sedimentary basins. Nature 2003;426:327-33.
74. Stahl DA, de la Torre JR. Physiology and diversity of ammoniaoxidizing Archaea. Annu Rev Microbiol 2012;66:83-101.
75. Stoddard SF, Smith BJ, Hein R, et al. rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res 2015;43:D593-8.
76. Takai K, Miyazaki M, Hirayama H, et al. Isolation and physiological characterization of two novel, piezophilic, thermophilic chemolithoautotrophs from a deep-sea hydrothermal vent chimney. Environ Microbiol 2009;11:1983-97.
77. Valentine DL. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nature Rev Microbiol 2007;5: 316-23.
78. Webster G, Blazejak A, Cragg BA, et al. Subsurface microbiology and biogeochemistry of a deep, cold-water carbonatemound from the Porcupine Seabight IODP Expedition 307. EnvironMicrobiol 2009;11:239-57.
79. Webster G, Newberry CJ, Fry JC, et al. Assessment of bacterial community structure in the deep sub- seafloor biosphere by 16S rDNA-based techniques: a cautionary tale. J Microbiol Meth 2003;55:155-64.
80. Webster G, Parkes RJ, Cragg BA, et al. Prokaryotic community composition and biogeochemical processes in deep subseafloor sediments from the Peru Margin. FEMS Microbiol Ecol 2006;58:65-85.
81. Webster G, Rinna J, Roussel EG, et al. Prokaryotic functional diversity in different biogeochemical depth zones in tidal sediments of the Severn Estuary, UK, revealed by stable-isotope probing. FEMS Microbiol Ecol 2010;72:179-97.
82. Webster G, Sullivan LA, Meng Y, et al. Archaeal community diversity and abundance changes along a natural salinity gradient in estuarine sediments. FEMS Microbiol Ecol 2015;91:1-18.
83. Wellsbury P, Herbert RA, Parkes RJ. Bacterial [methyl-H- 3]thymidine incorporation in substrate-amended estuarine sediment slurries. FEMS Microbiol Ecol 1994;15:237-48.
84. Wery N, Moricet JM, CueffV, et al. Caloranaerobacter azorensis gen. nov., sp. nov., an anaerobic thermophilic bacterium isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 2001;51:1789-96.
85. Weston NB, Joye SB. Temperature-driven decoupling of key phases of organic matter degradation in marine sediments. P Natl Acad Sci USA 2005;102:17036-40.
86. Whiticar MJ. Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane. Chem Geol 1999;161:291-314.
87. Yanagawa K, Morono Y, de Beer D, et al. Metabolically active microbial communities in marine sediment under high-CO2 and low-pH extremes. ISME J 2013;7:555-67.
88. Zeikus JG, Wolfe RS. Methanobacterium thermoautotrophicus sp n, an anaerobic, autotrophic, extreme thermophile. J Bacteriol 1972;109:707-13.