Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate-reducing benthic microbial populations

Saad S, Bhatnagar S, Tegetmeyer H, Geelhoed JS, Strous M, Ruff SE (2017)
ENVIRONMENTAL MICROBIOLOGY 19(12): 4866-4881.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Saad, Sainab; Bhatnagar, Srijak; Tegetmeyer, HalinaUniBi ; Geelhoed, Jeanine S.; Strous, Marc; Ruff, S. Emil
Abstract / Bemerkung
For the anaerobic remineralization of organic matter in marine sediments, sulfate reduction coupled to fermentation plays a key role. Here, we enriched sulfate-reducing/fermentative communities from intertidal sediments under defined conditions in continuous culture. We transiently exposed the cultures to oxygen or nitrate twice daily and investigated the community response. Chemical measurements, provisional genomes and transcriptomic profiles revealed trophic networks of microbial populations. Sulfate reducers coexisted with facultative nitrate reducers or aerobes enabling the community to adjust to nitrate or oxygen pulses. Exposure to oxygen and nitrate impacted the community structure, but did not suppress fermentation or sulfate reduction as community functions, highlighting their stability under dynamic conditions. The most abundant sulfate reducer in all cultures, related to Desulfotignum balticum, appeared to have coupled both acetate- and hydrogen oxidation to sulfate reduction. We describe a novel representative of the widespread uncultured candidate phylum Fermentibacteria (formerly candidate division Hyd24-12). For this strictly anaerobic, obligate fermentative bacterium, we propose the name (U)Sabulitectum silens' and identify it as a partner of sulfate reducers in marine sediments. Overall, we provide insights into the function of fermentative, as well as sulfate-reducing microbial communities and their adaptation to a dynamic environment.
Erscheinungsjahr
2017
Zeitschriftentitel
ENVIRONMENTAL MICROBIOLOGY
Band
19
Ausgabe
12
Seite(n)
4866-4881
ISSN
1462-2912
eISSN
1462-2920
Page URI
https://pub.uni-bielefeld.de/record/2917180

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Saad S, Bhatnagar S, Tegetmeyer H, Geelhoed JS, Strous M, Ruff SE. Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate-reducing benthic microbial populations. ENVIRONMENTAL MICROBIOLOGY. 2017;19(12):4866-4881.
Saad, S., Bhatnagar, S., Tegetmeyer, H., Geelhoed, J. S., Strous, M., & Ruff, S. E. (2017). Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate-reducing benthic microbial populations. ENVIRONMENTAL MICROBIOLOGY, 19(12), 4866-4881. doi:10.1111/1462-2920.13895
Saad, Sainab, Bhatnagar, Srijak, Tegetmeyer, Halina, Geelhoed, Jeanine S., Strous, Marc, and Ruff, S. Emil. 2017. “Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate-reducing benthic microbial populations”. ENVIRONMENTAL MICROBIOLOGY 19 (12): 4866-4881.
Saad, S., Bhatnagar, S., Tegetmeyer, H., Geelhoed, J. S., Strous, M., and Ruff, S. E. (2017). Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate-reducing benthic microbial populations. ENVIRONMENTAL MICROBIOLOGY 19, 4866-4881.
Saad, S., et al., 2017. Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate-reducing benthic microbial populations. ENVIRONMENTAL MICROBIOLOGY, 19(12), p 4866-4881.
S. Saad, et al., “Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate-reducing benthic microbial populations”, ENVIRONMENTAL MICROBIOLOGY, vol. 19, 2017, pp. 4866-4881.
Saad, S., Bhatnagar, S., Tegetmeyer, H., Geelhoed, J.S., Strous, M., Ruff, S.E.: Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate-reducing benthic microbial populations. ENVIRONMENTAL MICROBIOLOGY. 19, 4866-4881 (2017).
Saad, Sainab, Bhatnagar, Srijak, Tegetmeyer, Halina, Geelhoed, Jeanine S., Strous, Marc, and Ruff, S. Emil. “Transient exposure to oxygen or nitrate reveals ecophysiology of fermentative and sulfate-reducing benthic microbial populations”. ENVIRONMENTAL MICROBIOLOGY 19.12 (2017): 4866-4881.

77 References

Daten bereitgestellt von Europe PubMed Central.

Bioturbation and remineralization of sedimentary organic matter: effects of redox oscillation
AUTHOR UNKNOWN, 1994
Colloquium paper: resistance, resilience, and redundancy in microbial communities.
Allison SD, Martiny JB., Proc. Natl. Acad. Sci. U.S.A. 105 Suppl 1(), 2008
PMID: 18695234
Biochemistry, physiology and biotechnology of sulfate-reducing bacteria.
Barton LL, Fauque GD., Adv. Appl. Microbiol. 68(), 2009
PMID: 19426853
A historic perspective on Wadden Sea eutrophication
AUTHOR UNKNOWN, 2005
Surficial and deep pore water circulation governs spatial and temporal scales of nutrient recycling in intertidal sand flat sediment
AUTHOR UNKNOWN, 2006
Riverine nitrogen export from the continents to the coasts
AUTHOR UNKNOWN, 2006
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota.
Campbell JH, O'Donoghue P, Campbell AG, Schwientek P, Sczyrba A, Woyke T, Soll D, Podar M., Proc. Natl. Acad. Sci. U.S.A. 110(14), 2013
PMID: 23509275
Pathways of organic carbon oxidation in three continental margin sediments.
Canfield DE, Jorgensen BB, Fossing H, Glud R, Gundersen J, Ramsing NB, Thamdrup B, Hansen JW, Nielsen LP, Hall PO, Canfield DE., Mar. Geol. 113(), 1993
PMID: 11539842
Microbial methane cycling in a terrestrial mud volcano in eastern Taiwan.
Chang YH, Cheng TW, Lai WJ, Tsai WY, Sun CH, Lin LH, Wang PL., Environ. Microbiol. 14(4), 2011
PMID: 22141749
Impacts of chemical gradients on microbial community structure.
Chen J, Hanke A, Tegetmeyer HE, Kattelmann I, Sharma R, Hamann E, Hargesheimer T, Kraft B, Lenk S, Geelhoed JS, Hettich RL, Strous M., ISME J 11(4), 2017
PMID: 28094795
Spectrophotometric determination of hydrogen sulfide in natural waters
AUTHOR UNKNOWN, 1969
Microbial communities acclimate to recurring changes in soil redox potential status.
DeAngelis KM, Silver WL, Thompson AW, Firestone MK., Environ. Microbiol. 12(12), 2010
PMID: 20629704
Microbial Communities in Methane- and Short Chain Alkane-Rich Hydrothermal Sediments of Guaymas Basin.
Dowell F, Cardman Z, Dasarathy S, Kellermann MY, Lipp JS, Ruff SE, Biddle JF, McKay LJ, MacGregor BJ, Lloyd KG, Albert DB, Mendlovitz H, Hinrichs KU, Teske A., Front Microbiol 7(), 2016
PMID: 26858698
Phylogenetic and metabolic diversity of Planctomycetes from anaerobic, sulfide- and sulfur-rich Zodletone Spring, Oklahoma.
Elshahed MS, Youssef NH, Luo Q, Najar FZ, Roe BA, Sisk TM, Buhring SI, Hinrichs KU, Krumholz LR., Appl. Environ. Microbiol. 73(15), 2007
PMID: 17545322
Isolation of sulfate-reducing bacteria from sediments above the deep-subseafloor aquifer.
Fichtel K, Mathes F, Konneke M, Cypionka H, Engelen B., Front Microbiol 3(), 2012
PMID: 22363336
Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis
AUTHOR UNKNOWN, 1979
Intensive and extensive nitrogen loss from intertidal permeable sediments of the Wadden Sea
AUTHOR UNKNOWN, 2012
Recoding of the stop codon UGA to glycine by a BD1-5/SN-2 bacterium and niche partitioning between Alpha- and Gammaproteobacteria in a tidal sediment microbial community naturally selected in a laboratory chemostat.
Hanke A, Hamann E, Sharma R, Geelhoed JS, Hargesheimer T, Kraft B, Meyer V, Lenk S, Osmers H, Wu R, Makinwa K, Hettich RL, Banfield JF, Tegetmeyer HE, Strous M., Front Microbiol 5(), 2014
PMID: 24904545
Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat.
Harris JK, Caporaso JG, Walker JJ, Spear JR, Gold NJ, Robertson CE, Hugenholtz P, Goodrich J, McDonald D, Knights D, Marshall P, Tufo H, Knight R, Pace NR., ISME J 7(1), 2012
PMID: 22832344
The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough.
Heidelberg JF, Seshadri R, Haveman SA, Hemme CL, Paulsen IT, Kolonay JF, Eisen JA, Ward N, Methe B, Brinkac LM, Daugherty SC, Deboy RT, Dodson RJ, Durkin AS, Madupu R, Nelson WC, Sullivan SA, Fouts D, Haft DH, Selengut J, Peterson JD, Davidsen TM, Zafar N, Zhou L, Radune D, Dimitrov G, Hance M, Tran K, Khouri H, Gill J, Utterback TR, Feldblyum TV, Wall JD, Voordouw G, Fraser CM., Nat. Biotechnol. 22(5), 2004
PMID: 15077118
Anaerobic mineralization of marine sediment organic matter: rates and the role of anaerobic processes in the oceanic carbon economy
AUTHOR UNKNOWN, 1987
Carbon flow through oxygen and sulfate reduction pathways in salt marsh sediments
AUTHOR UNKNOWN, 1984
Pore‐water advection and solute fluxes in permeable marine sediments (II): benthic respiration at three sandy sites with different permeabilities (German Bight, North Sea)
AUTHOR UNKNOWN, 2005
Mineralization of organic matter in the sea bed ‐ the role of sulphate reduction
AUTHOR UNKNOWN, 1982
Dynamics of zero‐valent sulfur species including polysulfides at seep sites on intertidal sand flats (Wadden Sea, North Sea)
AUTHOR UNKNOWN, 2010
Genomic insights into members of the candidate phylum Hyd24-12 common in mesophilic anaerobic digesters.
Kirkegaard RH, Dueholm MS, McIlroy SJ, Nierychlo M, Karst SM, Albertsen M, Nielsen PH., ISME J 10(10), 2016
PMID: 27058503
Uncultivated microbes in need of their own taxonomy
AUTHOR UNKNOWN, 0
Rapid succession of uncultured marine bacterial and archaeal populations in a denitrifying continuous culture.
Kraft B, Tegetmeyer HE, Meier D, Geelhoed JS, Strous M., Environ. Microbiol. 16(10), 2014
PMID: 24976559
ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences.
Laslett D, Canback B., Nucleic Acids Res. 32(1), 2004
PMID: 14704338
Novel groups of Gammaproteobacteria catalyse sulfur oxidation and carbon fixation in a coastal, intertidal sediment.
Lenk S, Arnds J, Zerjatke K, Musat N, Amann R, Mussmann M., Environ. Microbiol. 13(3), 2010
PMID: 21134098
Phylogenetic analysis of five strains of gram‐negative, obligately anaerobic, sulfur‐reducing bacteria and description of Desulfuromusa gen. nov., Including Desulfuromusa kysingii sp. nov., Desulfuromusa bakii sp. nov., and Desulfuromusa succinoxidans sp
AUTHOR UNKNOWN, 1994
Community structure and activity of sulfate‐reducing bacteria in an intertidal surface sediment: a multi‐method approach
AUTHOR UNKNOWN, 2002
ARB: a software environment for sequence data.
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar , Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH., Nucleic Acids Res. 32(4), 2004
PMID: 14985472
Dominant microbial populations in limestone-corroding stream biofilms, Frasassi cave system, Italy.
Macalady JL, Lyon EH, Koffman B, Albertson LK, Meyer K, Galdenzi S, Mariani S., Appl. Environ. Microbiol. 72(8), 2006
PMID: 16885314
Thermal and geochemical influences on microbial biogeography in the hydrothermal sediments of Guaymas Basin, Gulf of California.
McKay L, Klokman VW, Mendlovitz HP, LaRowe DE, Hoer DR, Albert D, Amend JP, Teske A., Environ Microbiol Rep 8(1), 2016
PMID: 26637109
The fate of nitrate in intertidal permeable sediments.
Marchant HK, Lavik G, Holtappels M, Kuypers MM., PLoS ONE 9(8), 2014
PMID: 25127459
EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data.
Miller CS, Baker BJ, Thomas BC, Singer SW, Banfield JF., Genome Biol. 12(5), 2011
PMID: 21595876
The past and present of sodium energetics: may the sodium-motive force be with you.
Mulkidjanian AY, Dibrov P, Galperin MY., Biochim. Biophys. Acta 1777(7-8), 2008
PMID: 18485887
The ecology and biotechnology of sulphate-reducing bacteria.
Muyzer G, Stams AJ., Nat. Rev. Microbiol. 6(6), 2008
PMID: 18461075
Diurnal redox fluctuation and microbial activity in the rhizosphere of wetland plants
AUTHOR UNKNOWN, 2008
Diversity and spatial distribution of prokaryotic communities along a sediment vertical profile of a deep-sea mud volcano.
Pachiadaki MG, Kallionaki A, Dahlmann A, De Lange GJ, Kormas KA., Microb. Ecol. 62(3), 2011
PMID: 21538105
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes.
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW., Genome Res. 25(7), 2015
PMID: 25977477
Redox fluctuation structures microbial communities in a wet tropical soil.
Pett-Ridge J, Firestone MK., Appl. Environ. Microbiol. 71(11), 2005
PMID: 16269735
SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes.
Pruesse E, Peplies J, Glockner FO., Bioinformatics 28(14), 2012
PMID: 22556368
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO., Nucleic Acids Res. 41(Database issue), 2012
PMID: 23193283

AUTHOR UNKNOWN, 2013
Membrane-bound oxygen reductases of the anaerobic sulfate-reducing Desulfovibrio vulgaris Hildenborough: roles in oxygen defence and electron link with periplasmic hydrogen oxidation.
Ramel F, Amrani A, Pieulle L, Lamrabet O, Voordouw G, Seddiki N, Brethes D, Company M, Dolla A, Brasseur G., Microbiology (Reading, Engl.) 159(Pt 12), 2013
PMID: 24085836
Global dispersion and local diversification of the methane seep microbiome.
Ruff SE, Biddle JF, Teske AP, Knittel K, Boetius A, Ramette A., Proc. Natl. Acad. Sci. U.S.A. 112(13), 2015
PMID: 25775520
Methane Seep in Shallow-Water Permeable Sediment Harbors High Diversity of Anaerobic Methanotrophic Communities, Elba, Italy.
Ruff SE, Kuhfuss H, Wegener G, Lott C, Ramette A, Wiedling J, Knittel K, Weber M., Front Microbiol 7(), 2016
PMID: 27065954
Oxidative and reductive acetyl CoA/carbon monoxide dehydrogenase pathway in Desulfobacterium autotrophicum
AUTHOR UNKNOWN, 1988
Bacterial sulfur cycling shapes microbial communities in surface sediments of an ultramafic hydrothermal vent field.
Schauer R, Roy H, Augustin N, Gennerich HH, Peters M, Wenzhoefer F, Amann R, Meyerdierks A., Environ. Microbiol. 13(10), 2011
PMID: 21895907
Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea.
Schottner S, Pfitzner B, Grunke S, Rasheed M, Wild C, Ramette A., Environ. Microbiol. 13(7), 2011
PMID: 21554515
Prokka: rapid prokaryotic genome annotation.
Seemann T., Bioinformatics 30(14), 2014
PMID: 24642063
Fundamentals of microbial community resistance and resilience.
Shade A, Peter H, Allison SD, Baho DL, Berga M, Burgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JB, Matulich KL, Schmidt TM, Handelsman J., Front Microbiol 3(), 2012
PMID: 23267351
Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms.
Simister RL, Deines P, Botte ES, Webster NS, Taylor MW., Environ. Microbiol. 14(2), 2011
PMID: 22151434
Effects of oxygen and redox oscillation on degradation of cell‐associated lipids in surficial marine sediments
AUTHOR UNKNOWN, 2002
Importance of continental margins in the marine biogeochemical cycling of carbon and nitrogen
AUTHOR UNKNOWN, 1991
Microbial community dynamics in Inferno Crater Lake, a thermally fluctuating geothermal spring.
Ward L, Taylor MW, Power JF, Scott BJ, McDonald IR, Stott MB., ISME J 11(5), 2017
PMID: 28072418
Challenges in microbial ecology: building predictive understanding of community function and dynamics.
Widder S, Allen RJ, Pfeiffer T, Curtis TP, Wiuf C, Sloan WT, Cordero OX, Brown SP, Momeni B, Shou W, Kettle H, Flint HJ, Haas AF, Laroche B, Kreft JU, Rainey PB, Freilich S, Schuster S, Milferstedt K, van der Meer JR, Groβkopf T, Huisman J, Free A, Picioreanu C, Quince C, Klapper I, Labarthe S, Smets BF, Wang H; Isaac Newton Institute Fellows, Soyer OS., ISME J 10(11), 2016
PMID: 27022995
Enhanced biological phosphorus removal by granular sludge: from macro- to micro-scale.
Wu CY, Peng YZ, Wang SY, Ma Y., Water Res. 44(3), 2009
PMID: 19913871
Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences.
Yarza P, Yilmaz P, Pruesse E, Glockner FO, Ludwig W, Schleifer KH, Whitman WB, Euzeby J, Amann R, Rossello-Mora R., Nat. Rev. Microbiol. 12(9), 2014
PMID: 25118885
DNA recovery from soils of diverse composition.
Zhou J, Bruns MA, Tiedje JM., Appl. Environ. Microbiol. 62(2), 1996
PMID: 8593035
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