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Title: Microbial communities from Arctic marine sediments respond slowly to methane addition during ex situ enrichments

Abstract

Summary Anaerobic methanotrophic archaea (ANME) consume methane in marine sediments, limiting its release to the water column, but their responses to changes in methane and sulfate supplies remain poorly constrained. To address how methane exposure may affect microbial communities and methane‐ and sulfur‐cycling gene abundances in Arctic marine sediments, we collected sediments from offshore Svalbard that represent geochemical horizons where anaerobic methanotrophy is expected to be active, previously active, and long‐inactive based on reaction‐transport biogeochemical modelling of porewater sulfate profiles. Sediment slurries were incubated at in situ temperature and pressure with different added methane concentrations. Sediments from an active area of seepage began to reduce sulfate in a methane‐dependent manner within months, preceding increased relative abundances of anaerobic methanotrophs ANME‐1 within communities. In previously active and long‐inactive sediments, sulfur‐cycling Deltaproteobacteria became more dominant after 30 days, though these communities showed no evidence of methanotrophy after nearly 8 months of enrichment. Overall, enrichment conditions, but not methane, broadly altered microbial community structure across different enrichment times and sediment types. These results suggest that active ANME populations may require years to develop, and consequently microbial community composition may affect methanotrophic responses to potential large‐scale seafloor methane releases in ways that provide insight formore » future modelling studies.« less

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2];  [1]; ORCiD logo [3]; ORCiD logo [1]
  1. Oregon State Univ., Corvallis, OR (United States)
  2. Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography
  3. UiT The Arctic Univ. of Norway, Tromso (Norway)
Publication Date:
Research Org.:
Oregon State Univ., Corvallis, OR (United States)
Sponsoring Org.:
USDOE Office of Fossil Energy (FE); Research Council of Norway (RCN); USDOE
OSTI Identifier:
1799761
Alternate Identifier(s):
OSTI ID: 1582474
Grant/Contract Number:  
FE0013531; 223259; DE‐FE0013531
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 22; Journal Issue: 5; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; methane; AOM; sulfate reduction; marine sediments; Arctic; microbial communities; pressure enrichment

Citation Formats

Klasek, Scott, Torres, Marta E., Bartlett, Douglas H., Tyler, Madeline, Hong, Wei‐Li, and Colwell, Frederick. Microbial communities from Arctic marine sediments respond slowly to methane addition during ex situ enrichments. United States: N. p., 2019. Web. doi:10.1111/1462-2920.14895.
Klasek, Scott, Torres, Marta E., Bartlett, Douglas H., Tyler, Madeline, Hong, Wei‐Li, & Colwell, Frederick. Microbial communities from Arctic marine sediments respond slowly to methane addition during ex situ enrichments. United States. https://doi.org/10.1111/1462-2920.14895
Klasek, Scott, Torres, Marta E., Bartlett, Douglas H., Tyler, Madeline, Hong, Wei‐Li, and Colwell, Frederick. Sun . "Microbial communities from Arctic marine sediments respond slowly to methane addition during ex situ enrichments". United States. https://doi.org/10.1111/1462-2920.14895. https://www.osti.gov/servlets/purl/1799761.
@article{osti_1799761,
title = {Microbial communities from Arctic marine sediments respond slowly to methane addition during ex situ enrichments},
author = {Klasek, Scott and Torres, Marta E. and Bartlett, Douglas H. and Tyler, Madeline and Hong, Wei‐Li and Colwell, Frederick},
abstractNote = {Summary Anaerobic methanotrophic archaea (ANME) consume methane in marine sediments, limiting its release to the water column, but their responses to changes in methane and sulfate supplies remain poorly constrained. To address how methane exposure may affect microbial communities and methane‐ and sulfur‐cycling gene abundances in Arctic marine sediments, we collected sediments from offshore Svalbard that represent geochemical horizons where anaerobic methanotrophy is expected to be active, previously active, and long‐inactive based on reaction‐transport biogeochemical modelling of porewater sulfate profiles. Sediment slurries were incubated at in situ temperature and pressure with different added methane concentrations. Sediments from an active area of seepage began to reduce sulfate in a methane‐dependent manner within months, preceding increased relative abundances of anaerobic methanotrophs ANME‐1 within communities. In previously active and long‐inactive sediments, sulfur‐cycling Deltaproteobacteria became more dominant after 30 days, though these communities showed no evidence of methanotrophy after nearly 8 months of enrichment. Overall, enrichment conditions, but not methane, broadly altered microbial community structure across different enrichment times and sediment types. These results suggest that active ANME populations may require years to develop, and consequently microbial community composition may affect methanotrophic responses to potential large‐scale seafloor methane releases in ways that provide insight for future modelling studies.},
doi = {10.1111/1462-2920.14895},
journal = {Environmental Microbiology},
number = 5,
volume = 22,
place = {United States},
year = {Sun Dec 15 00:00:00 EST 2019},
month = {Sun Dec 15 00:00:00 EST 2019}
}

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Works referenced in this record:

Identification and Removal of Contaminant Sequences From Ribosomal Gene Databases: Lessons From the Census of Deep Life
journal, April 2018


Statistical Methods for Detecting Differentially Abundant Features in Clinical Metagenomic Samples
journal, April 2009


Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters
journal, May 1969


Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics
journal, October 2015


Effect of pressure and temperature on anaerobic methanotrophic activities of a highly enriched ANME-2a community
journal, June 2018

  • Bhattarai, Susma; Zhang, Yu; Lens, Piet N. L.
  • Environmental Science and Pollution Research, Vol. 25, Issue 30
  • DOI: 10.1007/s11356-018-2573-2

Improved measurement of microbial activity in deep-sea sediments at in situ pressure and methane concentration: Measuring activity in deep-sea sediments
journal, October 2011

  • Bowles, Marshall W.; Samarkin, Vladimir A.; Joye, Samantha B.
  • Limnology and Oceanography: Methods, Vol. 9, Issue 10
  • DOI: 10.4319/lom.2011.9.499

Relaxed Neighbor Joining: A Fast Distance-Based Phylogenetic Tree Construction Method
journal, April 2006

  • Evans, Jason; Sheneman, Luke; Foster, James
  • Journal of Molecular Evolution, Vol. 62, Issue 6
  • DOI: 10.1007/s00239-005-0176-2

In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate
journal, January 2007


Stimulation of in vitro anaerobic oxidation of methane rate in a continuous high-pressure bioreactor
journal, May 2010


Experimental Incubations Elicit Profound Changes in Community Transcription in OMZ Bacterioplankton
journal, May 2012


Variations in Archaeal and Bacterial Diversity Associated with the Sulfate-Methane Transition Zone in Continental Margin Sediments (Santa Barbara Basin, California)
journal, January 2009

  • Harrison, B. K.; Zhang, H.; Berelson, W.
  • Applied and Environmental Microbiology, Vol. 75, Issue 6
  • DOI: 10.1128/AEM.01812-08

Global dispersion and local diversification of the methane seep microbiome
journal, March 2015

  • Ruff, S. Emil; Biddle, Jennifer F.; Teske, Andreas P.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 13
  • DOI: 10.1073/pnas.1421865112

Effects of climate change on methane emissions from seafloor sediments in the Arctic Ocean: A review: Methane Emissions from Arctic Sediments
journal, May 2016

  • James, Rachael H.; Bousquet, Philippe; Bussmann, Ingeborg
  • Limnology and Oceanography, Vol. 61, Issue S1
  • DOI: 10.1002/lno.10307

Enrichment of anaerobic methanotrophs in sulfate-reducing membrane bioreactors
journal, October 2009

  • Meulepas, Roel J. W.; Jagersma, Christian G.; Gieteling, Jarno
  • Biotechnology and Bioengineering, Vol. 104, Issue 3
  • DOI: 10.1002/bit.22412

Seepage from an arctic shallow marine gas hydrate reservoir is insensitive to momentary ocean warming
journal, June 2017

  • Hong, Wei-Li; Torres, Marta E.; Carroll, JoLynn
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms15745

Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform
journal, June 2013

  • Kozich, James J.; Westcott, Sarah L.; Baxter, Nielson T.
  • Applied and Environmental Microbiology, Vol. 79, Issue 17
  • DOI: 10.1128/AEM.01043-13

Precise δ 13 C analysis of dissolved inorganic carbon in natural waters using automated headspace sampling and continuous-flow mass spectrometry. : Automated δ
journal, August 2005

  • Torres, Marta E.; Mix, Alan C.; Rugh, William D.
  • Limnology and Oceanography: Methods, Vol. 3, Issue 8
  • DOI: 10.4319/lom.2005.3.349

Carbon isotope equilibration during sulphate-limited anaerobic oxidation of methane
journal, January 2014

  • Yoshinaga, Marcos Y.; Holler, Thomas; Goldhammer, Tobias
  • Nature Geoscience, Vol. 7, Issue 3
  • DOI: 10.1038/ngeo2069

Quantitative and Qualitative   Diversity Measures Lead to Different Insights into Factors That Structure Microbial Communities
journal, January 2007

  • Lozupone, C. A.; Hamady, M.; Kelley, S. T.
  • Applied and Environmental Microbiology, Vol. 73, Issue 5
  • DOI: 10.1128/AEM.01996-06

Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review
journal, January 2002


Control of sulfate pore-water profiles by sedimentary events and the significance of anaerobic oxidation of methane for the burial of sulfur in marine sediments
journal, July 2003


Kinetics of growth, substrate utilization and sulfide toxicity for propionate, acetate, and hydrogen utilizers in anaerobic systems
journal, November 1996

  • Maillacheruvu, Krishnanand Y.; Parkin, Gene F.
  • Water Environment Research, Vol. 68, Issue 7
  • DOI: 10.2175/106143096X128126

Characterization of Microbial Population Shifts during Sample Storage
journal, January 2012


Methane efflux from marine sediments in passive and active margins: Estimations from bioenergetic reaction–transport simulations
journal, January 2008

  • Dale, A. W.; Van Cappellen, P.; Aguilera, D. R.
  • Earth and Planetary Science Letters, Vol. 265, Issue 3-4
  • DOI: 10.1016/j.epsl.2007.09.026

Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010

  • Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
  • DOI: 10.1073/pnas.1000080107

Detection and Enumeration of Sulphate-Reducing Bacteria in Estuarine Sediments by Competitive PCR
journal, April 2004


Methanogenic activity and diversity in the centre of the Amsterdam Mud Volcano, Eastern Mediterranean Sea
journal, April 2012


Reagent and laboratory contamination can critically impact sequence-based microbiome analyses
journal, November 2014


The active methanotrophic community in hydromorphic soils changes in response to changing methane concentration
journal, February 2006


Draconibacterium orientale gen. nov., sp. nov., isolated from two distinct marine environments, and proposal of Draconibacteriaceae fam. nov.
journal, February 2014

  • Du, Z. -J.; Wang, Y.; Dunlap, C.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 5
  • DOI: 10.1099/ijs.0.056812-0

Metabolic Capabilities of Microorganisms Involved in and Associated with the Anaerobic Oxidation of Methane
journal, February 2016


Anaerobic Oxidation of Methane: Progress with an Unknown Process
journal, October 2009


Non-parametric multivariate analyses of changes in community structure
journal, March 1993


Desulfuromonas svalbardensis sp. nov. and Desulfuromusa ferrireducens sp. nov., psychrophilic, Fe(III)-reducing bacteria isolated from Arctic sediments, Svalbard
journal, May 2006

  • Vandieken, V.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 5
  • DOI: 10.1099/ijs.0.63639-0

Oceanic Methane Biogeochemistry
journal, February 2007


Methane dynamics in a microbial community of the Black Sea traced by stable carbon isotopes in vitro
journal, October 2006


The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

Enrichment of ANME-2 dominated anaerobic methanotrophy from cold seep sediment in an external ultrafiltration membrane bioreactor
journal, March 2018

  • Bhattarai, Susma; Cassarini, Chiara; Rene, Eldon R.
  • Engineering in Life Sciences, Vol. 18, Issue 6
  • DOI: 10.1002/elsc.201700148

In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area
journal, May 2002


Dynamic interactions between iron and sulfur cycles from Arctic methane seeps
journal, May 2018

  • Latour, Pauline; Hong, Wei-Li; Sauer, Simone
  • Biogeosciences Discussions
  • DOI: 10.5194/bg-2018-223

Identification of Methyl Coenzyme M Reductase A (mcrA) Genes Associated with Methane-Oxidizing Archaea
journal, September 2003


Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments
journal, April 2019


The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill b
journal, November 2002


Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage
journal, July 2013

  • Haroon, Mohamed F.; Hu, Shihu; Shi, Ying
  • Nature, Vol. 500, Issue 7464
  • DOI: 10.1038/nature12375

Sulfidogenesis from 2-Aminoethanesulfonate (Taurine) Fermentation by a Morphologically Unusual Sulfate-Reducing Bacterium,Desulforhopalus singaporensis sp. nov.
journal, January 1999


Growth and Population Dynamics of Anaerobic Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in a Continuous-Flow Bioreactor
journal, July 2005


Microbial community assembly and evolution in subseafloor sediment
journal, February 2017

  • Starnawski, Piotr; Bataillon, Thomas; Ettema, Thijs J. G.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 11
  • DOI: 10.1073/pnas.1614190114

Stratified Community Responses to Methane and Sulfate Supplies in Mud Volcano Deposits: Insights from an In Vitro Experiment
journal, November 2014


Critical Evaluation of the Volumetric "Bottle Effect" on Microbial Batch Growth
journal, December 2009

  • Hammes, F.; Vital, M.; Egli, T.
  • Applied and Environmental Microbiology, Vol. 76, Issue 4
  • DOI: 10.1128/AEM.01914-09

Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

Postglacial response of Arctic Ocean gas hydrates to climatic amelioration
journal, June 2017

  • Serov, Pavel; Vadakkepuliyambatta, Sunil; Mienert, Jürgen
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 24
  • DOI: 10.1073/pnas.1619288114

High-pressure systems for gas-phase free continuous incubation of enriched marine microbial communities performing anaerobic oxidation of methane
journal, February 2010

  • Deusner, Christian; Meyer, Volker; Ferdelman, Timothy G.
  • Biotechnology and Bioengineering, Vol. 105, Issue 3
  • DOI: 10.1002/bit.22553

Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor
journal, September 2003


Tracing the slow growth of anaerobic methane-oxidizing communities by 15N-labelling techniques: 15N-labelling of anaerobic methanotrophs
journal, March 2008


Quantification of mcrA by fluorescent PCR in methanogenic and methanotrophic microbial communities: Quantification of mcrA by fluorescent PCR
journal, May 2008


Oxidation and incorporation of hydrogen sulfide by dissolved organic matter
journal, November 2006


Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota
journal, October 2016


Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle
journal, February 2018

  • Anantharaman, Karthik; Hausmann, Bela; Jungbluth, Sean P.
  • The ISME Journal, Vol. 12, Issue 7
  • DOI: 10.1038/s41396-018-0078-0

In situ development of a methanotrophic microbiome in deep-sea sediments
journal, August 2018


Methane dynamics regulated by microbial community response to permafrost thaw
journal, October 2014

  • McCalley, Carmody K.; Woodcroft, Ben J.; Hodgkins, Suzanne B.
  • Nature, Vol. 514, Issue 7523
  • DOI: 10.1038/nature13798

Organic Matter Loading Modifies the Microbial Community Responsible for Nitrogen Loss in Estuarine Sediments
journal, October 2015


Escape of methane gas from the seabed along the West Spitsbergen continental margin: ARCTIC METHANE GAS PLUMES
journal, August 2009

  • Westbrook, Graham K.; Thatcher, Kate E.; Rohling, Eelco J.
  • Geophysical Research Letters, Vol. 36, Issue 15
  • DOI: 10.1029/2009GL039191

Seafloor oxygen consumption fuelled by methane from cold seeps
journal, August 2013

  • Boetius, Antje; Wenzhöfer, Frank
  • Nature Geoscience, Vol. 6, Issue 9
  • DOI: 10.1038/ngeo1926

Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases
journal, October 2014

  • Müller, Albert Leopold; Kjeldsen, Kasper Urup; Rattei, Thomas
  • The ISME Journal, Vol. 9, Issue 5
  • DOI: 10.1038/ismej.2014.208

Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways
journal, December 2013


Deep-Sourced Fluids From a Convergent Margin Host Distinct Subseafloor Microbial Communities That Change Upon Mud Flow Expulsion
journal, June 2019


Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities
journal, January 2005


Marine pore-water sulfate profiles indicate in situ methane flux from underlying gas hydrate
journal, January 1996


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
journal, February 2009

  • Holmes, Dawn E.; Nicoll, Julie S.; Bond, Daniel R.
  • Applied and Environmental Microbiology, Vol. 75, Issue 3
  • DOI: 10.1128/aem.02619-08

Reagent and laboratory contamination can critically impact sequence-based microbiome analyses.
text, January 2014

  • Salter, Susannah; Cox, Michael J.; Turek, Elena M.
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.41109

Effects of climate change on methane emissions from seafloor sediments in the Arctic Ocean: A review
text, January 2016


Oceanic Methane Biogeochemistry
journal, May 2007


Global dispersion and local diversification of the methane seep microbiome
text, January 2015

  • Teske, Andreas P.; Ramette, Alban Nicolas; Boetius, Antje
  • National Academy of Sciences NAS
  • DOI: 10.7892/boris.91364