DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Molybdenum-Based Diazotrophy in a Sphagnum Peatland in Northern Minnesota

Abstract

Microbial N2fixation (diazotrophy) represents an important nitrogen source to oligotrophic peatland ecosystems, which are important sinks for atmospheric CO2 and are susceptible to the changing climate. The objectives of this study were (i) to determine the active microbial group and type of nitrogenase mediating diazotrophy in an ombrotrophicSphagnum-dominated peat bog (the S1 peat bog, Marcell Experimental Forest, Minnesota, USA); and (ii) to determine the effect of environmental parameters (light, O2, CO2, and CH4) on potential rates of diazotrophy measured by acetylene (C2H2) reduction and15N2incorporation. A molecular analysis of metabolically active microbial communities suggested that diazotrophy in surface peat was primarily mediated byAlphaproteobacteria(BradyrhizobiaceaeandBeijerinckiaceae). Despite higher concentrations of dissolved vanadium ([V] 11 nM) than molybdenum ([Mo] 3 nM) in surface peat, a combination of metagenomic, amplicon sequencing, and activity measurements indicated that Mo-containing nitrogenases dominate over the V-containing form. Acetylene reduction was only detected in surface peat exposed to light, with the highest rates observed in peat collected from hollows with the highest water contents. Incorporation of15N2was suppressed 90% by O2and 55% by C2H2and was unaffected by CH4and CO2amendments. These results suggest that peatland diazotrophy is mediated by a combination of C2H2-sensitive and C2H2-insensitive microbes that are more active at low concentrationsmore » of O2and show similar activity at high and low concentrations of CH4. IMPORTANCE Previous studies indicate that diazotrophy provides an important nitrogen source and is linked to methanotrophy inSphagnum-dominated peatlands. However, the environmental controls and enzymatic pathways of peatland diazotrophy, as well as the metabolically active microbial populations that catalyze this process, remain in question. Our findings indicate that oxygen levels and photosynthetic activity override low nutrient availability in limiting diazotrophy and that members of theAlphaproteobacteria(Rhizobiales) catalyze this process at the bog surface using the molybdenum-based form of the nitrogenase enzyme.« less

Authors:
 [1];  [2];  [2];  [1];  [2];  [3];  [4];  [5];  [5];  [6]; ORCiD logo [6]
  1. Georgia Inst. of Technology, Atlanta, GA (United States). School of Earth and Atmospheric Sciences
  2. Georgia Inst. of Technology, Atlanta, GA (United States). School of Biological Sciences
  3. Florida State Univ., Tallahassee, FL (United States). National High Magnetic Field Lab. (MagLab)
  4. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Physical and Life Sciences Directorate
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Divison
  6. Georgia Inst. of Technology, Atlanta, GA (United States). School of Earth and Atmospheric Sciences and School of Biological Sciences
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1394354
Alternate Identifier(s):
OSTI ID: 1478664
Report Number(s):
LLNL-JRNL-731618
Journal ID: ISSN 0099-2240
Grant/Contract Number:  
AC05-00OR22725; SC0007144; SC0012088; AC52-07NA27344
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 83; Journal Issue: 17; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Alphaproteobacteria; Sphagnum; acetylene; diazotrophy; methanotrophs; molybdenum; nitrogen cycle enzymes; nitrogen fixation; peatland; vanadium

Citation Formats

Warren, Melissa J., Lin, Xueju, Gaby, John C., Kretz, Cecilia B., Kolton, Max, Morton, Peter L., Pett-Ridge, Jennifer, Weston, David J., Schadt, Christopher W., Kostka, Joel E., and Glass, Jennifer B. Molybdenum-Based Diazotrophy in a Sphagnum Peatland in Northern Minnesota. United States: N. p., 2017. Web. doi:10.1128/AEM.01174-17.
Warren, Melissa J., Lin, Xueju, Gaby, John C., Kretz, Cecilia B., Kolton, Max, Morton, Peter L., Pett-Ridge, Jennifer, Weston, David J., Schadt, Christopher W., Kostka, Joel E., & Glass, Jennifer B. Molybdenum-Based Diazotrophy in a Sphagnum Peatland in Northern Minnesota. United States. https://doi.org/10.1128/AEM.01174-17
Warren, Melissa J., Lin, Xueju, Gaby, John C., Kretz, Cecilia B., Kolton, Max, Morton, Peter L., Pett-Ridge, Jennifer, Weston, David J., Schadt, Christopher W., Kostka, Joel E., and Glass, Jennifer B. Fri . "Molybdenum-Based Diazotrophy in a Sphagnum Peatland in Northern Minnesota". United States. https://doi.org/10.1128/AEM.01174-17. https://www.osti.gov/servlets/purl/1394354.
@article{osti_1394354,
title = {Molybdenum-Based Diazotrophy in a Sphagnum Peatland in Northern Minnesota},
author = {Warren, Melissa J. and Lin, Xueju and Gaby, John C. and Kretz, Cecilia B. and Kolton, Max and Morton, Peter L. and Pett-Ridge, Jennifer and Weston, David J. and Schadt, Christopher W. and Kostka, Joel E. and Glass, Jennifer B.},
abstractNote = {Microbial N2fixation (diazotrophy) represents an important nitrogen source to oligotrophic peatland ecosystems, which are important sinks for atmospheric CO2 and are susceptible to the changing climate. The objectives of this study were (i) to determine the active microbial group and type of nitrogenase mediating diazotrophy in an ombrotrophicSphagnum-dominated peat bog (the S1 peat bog, Marcell Experimental Forest, Minnesota, USA); and (ii) to determine the effect of environmental parameters (light, O2, CO2, and CH4) on potential rates of diazotrophy measured by acetylene (C2H2) reduction and15N2incorporation. A molecular analysis of metabolically active microbial communities suggested that diazotrophy in surface peat was primarily mediated byAlphaproteobacteria(BradyrhizobiaceaeandBeijerinckiaceae). Despite higher concentrations of dissolved vanadium ([V] 11 nM) than molybdenum ([Mo] 3 nM) in surface peat, a combination of metagenomic, amplicon sequencing, and activity measurements indicated that Mo-containing nitrogenases dominate over the V-containing form. Acetylene reduction was only detected in surface peat exposed to light, with the highest rates observed in peat collected from hollows with the highest water contents. Incorporation of15N2was suppressed 90% by O2and 55% by C2H2and was unaffected by CH4and CO2amendments. These results suggest that peatland diazotrophy is mediated by a combination of C2H2-sensitive and C2H2-insensitive microbes that are more active at low concentrations of O2and show similar activity at high and low concentrations of CH4. IMPORTANCE Previous studies indicate that diazotrophy provides an important nitrogen source and is linked to methanotrophy inSphagnum-dominated peatlands. However, the environmental controls and enzymatic pathways of peatland diazotrophy, as well as the metabolically active microbial populations that catalyze this process, remain in question. Our findings indicate that oxygen levels and photosynthetic activity override low nutrient availability in limiting diazotrophy and that members of theAlphaproteobacteria(Rhizobiales) catalyze this process at the bog surface using the molybdenum-based form of the nitrogenase enzyme.},
doi = {10.1128/AEM.01174-17},
journal = {Applied and Environmental Microbiology},
number = 17,
volume = 83,
place = {United States},
year = {Fri Jun 30 00:00:00 EDT 2017},
month = {Fri Jun 30 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 39 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Analysis of methanotrophic bacteria in Movile Cave by stable isotope probing: Methanotrophs in Movile Cave
journal, December 2003


Methanotrophs and copper
journal, July 2010


Attaining whole-ecosystem warming using air and deep-soil heating methods with an elevated CO 2 atmosphere
journal, January 2017

  • Hanson, Paul J.; Riggs, Jeffery S.; Nettles, W. Robert
  • Biogeosciences, Vol. 14, Issue 4
  • DOI: 10.5194/bg-14-861-2017

Methanotrophic symbionts provide carbon for photosynthesis in peat bogs
journal, August 2005

  • Raghoebarsing, Ashna A.; Smolders, Alfons J. P.; Schmid, Markus C.
  • Nature, Vol. 436, Issue 7054
  • DOI: 10.1038/nature03802

Classifying the metal dependence of uncharacterized nitrogenases
journal, January 2013


Effect of metal-binding agents and other compounds on methane oxidation by two strains of Methylococcus capsulatus
journal, January 1977

  • Stirling, David I.; Dalton, Howard
  • Archives of Microbiology, Vol. 114, Issue 1
  • DOI: 10.1007/BF00429633

A fast and direct spectrophotometric method for the sequential determination of nitrate and nitrite at low concentrations in small volumes
journal, May 2014


Acetylene as a suicide substrate and active site probe for methane monooxygenase from Methylococcus capsulatus (Bath)
journal, August 1985


Nitrogen cycling in a forested Minnesota bog
journal, March 1988

  • Urban, N. R.; Eisenreich, S. J.
  • Canadian Journal of Botany, Vol. 66, Issue 3
  • DOI: 10.1139/b88-069

Similar Diversity of Alphaproteobacteria and Nitrogenase Gene Amplicons on Two Related Sphagnum Mosses
journal, January 2012


Nitrogen Fixation in Wet Minerotrophic Moss Communities of a Subarctic Mire
journal, January 1978

  • Basilier, Karl; Granhall, Ulf; Stenström, Thor-Axel
  • Oikos, Vol. 31, Issue 2
  • DOI: 10.2307/3543568

The Natural History of Nitrogen Fixation
journal, March 2004

  • Raymond, Jason; Siefert, Janet L.; Staples, Christopher R.
  • Molecular Biology and Evolution, Vol. 21, Issue 3
  • DOI: 10.1093/molbev/msh047

Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil
journal, January 2001


Methanotrophy induces nitrogen fixation during peatland development
journal, December 2013

  • Larmola, T.; Leppanen, S. M.; Tuittila, E. -S.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 2
  • DOI: 10.1073/pnas.1314284111

RAPSearch2: a fast and memory-efficient protein similarity search tool for next-generation sequencing data
journal, October 2011


Diversity and Activity of Alternative Nitrogenases in Sequenced Genomes and Coastal Environments
journal, February 2017

  • McRose, Darcy L.; Zhang, Xinning; Kraepiel, Anne M. L.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.00267

Comparisons of soil nitrogen mass balances for an ombrotrophic bog and a minerotrophic fen in northern Minnesota
journal, April 2016


Effect of acetylene on autotrophic and heterotrophic nitrification
journal, March 1982

  • Hynes, R. K.; Knowles, R.
  • Canadian Journal of Microbiology, Vol. 28, Issue 3
  • DOI: 10.1139/m82-049

Storage and bioavailability of molybdenum in soils increased by organic matter complexation
journal, August 2009

  • Wichard, Thomas; Mishra, Bhoopesh; Myneni, Satish C. B.
  • Nature Geoscience, Vol. 2, Issue 9
  • DOI: 10.1038/ngeo589

Is vanadium a biometal for boreal cyanolichens?
journal, March 2014

  • Darnajoux, Romain; Constantin, Jérôme; Miadlikowska, Jolanta
  • New Phytologist, Vol. 202, Issue 3
  • DOI: 10.1111/nph.12777

The Sphagnum microbiome: new insights from an ancient plant lineage
journal, February 2016

  • Kostka, Joel E.; Weston, David J.; Glass, Jennifer B.
  • New Phytologist, Vol. 211, Issue 1
  • DOI: 10.1111/nph.13993

Microbial Metabolic Potential for Carbon Degradation and Nutrient (Nitrogen and Phosphorus) Acquisition in an Ombrotrophic Peatland
journal, March 2014

  • Lin, Xueju; Tfaily, Malak M.; Green, Stefan J.
  • Applied and Environmental Microbiology, Vol. 80, Issue 11
  • DOI: 10.1128/AEM.00206-14

Examining the impact of acetylene on N-fixation and the active sediment microbial community
journal, May 2015

  • Fulweiler, Robinson W.; Heiss, Elise M.; Rogener, Mary Kate
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00418

A modified single solution method for the determination of phosphate in natural waters
journal, January 1962


Microbial Community Structure and Activity Linked to Contrasting Biogeochemical Gradients in Bog and Fen Environments of the Glacial Lake Agassiz Peatland
journal, July 2012

  • Lin, X.; Green, S.; Tfaily, M. M.
  • Applied and Environmental Microbiology, Vol. 78, Issue 19
  • DOI: 10.1128/AEM.01750-12

Ethane formation from acetylene as a potential test for vanadium nitrogenase in vivo
journal, May 1987

  • Dilworth, Michael J.; Eady, Robert R.; Robson, Robert L.
  • Nature, Vol. 327, Issue 6118
  • DOI: 10.1038/327167a0

MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods
journal, May 2011

  • Tamura, K.; Peterson, D.; Peterson, N.
  • Molecular Biology and Evolution, Vol. 28, Issue 10
  • DOI: 10.1093/molbev/msr121

Nitrogen fixation and methanotrophy in forest mosses along a N deposition gradient
journal, June 2013


Possible contribution of alternative nitrogenases to nitrogen fixation by asymbiotic N2-fixing bacteria in soils
journal, February 2014


N2-fixation by methanotrophs sustains carbon and nitrogen accumulation in pristine peatlands
journal, August 2014


Nitrogenase gene diversity and microbial community structure: a cross-system comparison
journal, July 2003


Integrative analysis of environmental sequences using MEGAN4
journal, June 2011

  • Huson, D. H.; Mitra, S.; Ruscheweyh, H. -J.
  • Genome Research, Vol. 21, Issue 9
  • DOI: 10.1101/gr.120618.111

Methyloferula stellata gen. nov., sp. nov., an acidophilic, obligately methanotrophic bacterium that possesses only a soluble methane monooxygenase
journal, November 2010

  • Vorobev, A. V.; Baani, M.; Doronina, N. V.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 61, Issue 10
  • DOI: 10.1099/ijs.0.028118-0

Environmental distribution and abundance of the facultative methanotroph Methylocella
journal, December 2010


Nature of Oxygen Inhibition of Nitrogenase from Azotobacter vinelandii
journal, March 1972

  • Wong, P. P.; Burris, R. H.
  • Proceedings of the National Academy of Sciences, Vol. 69, Issue 3
  • DOI: 10.1073/pnas.69.3.672

Dynamic Vertical Profiles of Peat Porewater Chemistry in a Northern Peatland
journal, October 2016


S phagnum physiology in the context of changing climate: emergent influences of genomics, modelling and host-microbiome interactions on understanding ecosystem function
journal, December 2014

  • Weston, David J.; Timm, Collin M.; Walker, Anthony P.
  • Plant, Cell & Environment, Vol. 38, Issue 9
  • DOI: 10.1111/pce.12458

A comprehensive aligned nifH gene database: a multipurpose tool for studies of nitrogen-fixing bacteria
journal, January 2014


Significant nonsymbiotic nitrogen fixation in Patagonian ombrotrophic bogs
journal, March 2015

  • Knorr, Klaus-Holger; Horn, Marcus A.; Borken, Werner
  • Global Change Biology, Vol. 21, Issue 6
  • DOI: 10.1111/gcb.12849

Toxic effects of lab-grade butyl rubber stoppers on aerobic methane oxidation: Toxic effects of aerobic methane oxidation
journal, January 2015

  • Niemann, Helge; Steinle, Lea; Blees, Jan
  • Limnology and Oceanography: Methods, Vol. 13, Issue 1
  • DOI: 10.1002/lom3.10005

Acetylene Reduction by Beijerinckia under Various Partial Pressures of Oxygen and Acetylene
journal, October 1973


Molybdenum limitation of microbial nitrogen assimilation in aquatic ecosystems and pure cultures
journal, January 2012

  • Glass, Jennifer B.; Axler, Richard P.; Chandra, Sudeep
  • Frontiers in Microbiology, Vol. 3
  • DOI: 10.3389/fmicb.2012.00331

The Limits to Peat Bog Growth
journal, January 1984

  • Clymo, R. S.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 303, Issue 1117
  • DOI: 10.1098/rstb.1984.0002

The deposition of molybdenum in anoxic waters
journal, September 1972


Global prevalence of methane oxidation by symbiotic bacteria in peat-moss ecosystems
journal, August 2010

  • Kip, Nardy; van Winden, Julia F.; Pan, Yao
  • Nature Geoscience, Vol. 3, Issue 9
  • DOI: 10.1038/ngeo939

Isolation of Acidophilic Methane-Oxidizing Bacteria from Northern Peat Wetlands
journal, October 1998


Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA
journal, March 2014

  • Lin, Xueju; Tfaily, Malak M.; Steinweg, J. Megan
  • Applied and Environmental Microbiology, Vol. 80, Issue 11
  • DOI: 10.1128/AEM.00205-14

A Comprehensive Evaluation of PCR Primers to Amplify the nifH Gene of Nitrogenase
journal, July 2012


Peatlands and the carbon cycle: from local processes to global implications – a synthesis
journal, January 2008


Methylocella palustris gen. nov., sp. nov., a new methane-oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine-pathway methanotrophs
journal, May 2000

  • Dedysh, S. N.; Liesack, W.; Khmelenina, V. N.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 50, Issue 3
  • DOI: 10.1099/00207713-50-3-955

Nitrogen fixation in Sphagnum mosses is affected by moss species and water table level
journal, December 2014


Phylogenetic Comparison of the Methanogenic Communities from an Acidic, Oligotrophic Fen and an Anaerobic Digester Treating Municipal Wastewater Sludge
journal, September 2008

  • Steinberg, L. M.; Regan, J. M.
  • Applied and Environmental Microbiology, Vol. 74, Issue 21
  • DOI: 10.1128/AEM.00553-08

Active Methanotrophs in Two Contrasting North American Peatland Ecosystems Revealed Using DNA-SIP
journal, July 2011


Lichen-symbiotic cyanobacteria associated with Peltigera have an alternative vanadium-dependent nitrogen fixation system
journal, January 2014

  • Hodkinson, Brendan P.; Allen, Jessica L.; Forrest, Laura L.
  • European Journal of Phycology, Vol. 49, Issue 1
  • DOI: 10.1080/09670262.2013.873143

Influence of Dissolved Organic Matter On the Bio-Availability and Toxicity of Metals in Soils and Aquatic Systems
journal, December 1993


Conservation of nif sequences in Frankia
journal, August 1988

  • Normand, Philippe; Simonet, Pascal; Bardin, Ren�
  • MGG Molecular & General Genetics, Vol. 213, Issue 2-3
  • DOI: 10.1007/BF00339587

The Ecology of Sphagnum
book, January 1982


Long-term carbon sequestration in North American peatlands
journal, December 2012


Northern peatland carbon stocks and dynamics: a review
journal, January 2012


Diazotrophic methanotrophs in peatlands: the missing link?
journal, February 2015


The Acetylene-Ethylene Assay for N 2 Fixation: Laboratory and Field Evaluation
journal, August 1968

  • Hardy, R. W. F.; Holsten, R. D.; Jackson, E. K.
  • Plant Physiology, Vol. 43, Issue 8
  • DOI: 10.1104/pp.43.8.1185

The acetylene reduction technique as an assay for nitrogenase activity in the methane oxidizing bacterium Methylococcus capsulatus strain bath
journal, January 1976

  • Dalton, Howard; Whittenbury, Roger
  • Archives of Microbiology, Vol. 109, Issue 1-2
  • DOI: 10.1007/BF00425127

Vanadium and molybdenum requirement for the fixation of molecular nitrogen by two Methanosarcina strains
journal, December 1988


Nitrogenase Activity in Relation to Intracellular Organisms in Sphagnum Mosses
journal, January 1976


Detection, Isolation, and Characterization of Acidophilic Methanotrophs from Sphagnum Mosses
journal, July 2011

  • Kip, Nardy; Ouyang, Wenjing; van Winden, Julia
  • Applied and Environmental Microbiology, Vol. 77, Issue 16
  • DOI: 10.1128/AEM.05017-11

The Sphagnum microbiome supports bog ecosystem functioning under extreme conditions
journal, September 2014

  • Bragina, Anastasia; Oberauner-Wappis, Lisa; Zachow, Christin
  • Molecular Ecology, Vol. 23, Issue 18
  • DOI: 10.1111/mec.12885

Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP-PLFA analyses
journal, February 2008


Nitrogen Fixation in a Subarctic Mire
journal, January 1973

  • Granhall, Ulf; Selander, Hans
  • Oikos, Vol. 24, Issue 1
  • DOI: 10.2307/3543247

Some properties of a soluble methane mono-oxygenase from Methylococcus capsulatus strain Bath
journal, August 1976

  • Colby, J.; Dalton, H.
  • Biochemical Journal, Vol. 157, Issue 2
  • DOI: 10.1042/bj1570495

Transfer of fixed-N from N2-fixing cyanobacteria associated with the moss Sphagnum riparium results in enhanced growth of the moss
journal, May 2012


Applications of the acetylene-ethylene assay for measurement of nitrogen fixation
journal, January 1973


Trace-gas metabolic versatility of the facultative methanotroph Methylocella silvestris
journal, April 2014


Soil organic matter regulates molybdenum storage and mobility in forests
journal, July 2015


The composition of the continental crust
journal, April 1995


Nonsymbiotic and Symbiotic Nitrogen Fixation in a Weakly Minerotrophic Peatland
journal, August 1983

  • Schwintzer, Christa R.
  • American Journal of Botany, Vol. 70, Issue 7
  • DOI: 10.2307/2442817

Quantitative Detection of Methanotrophs in Soil by Novel pmoA-Targeted Real-Time PCR Assays
journal, May 2003


Characterization of Diazotrophs Containing Mo-Independent Nitrogenases, Isolated from Diverse Natural Environments
journal, March 2008

  • Betancourt, D. A.; Loveless, T. M.; Brown, J. W.
  • Applied and Environmental Microbiology, Vol. 74, Issue 11
  • DOI: 10.1128/AEM.02694-07

Molybdenum-nitrogen co-limitation in freshwater and coastal heterocystous cyanobacteria
journal, February 2010

  • Glass, Jennifer B.; Wolfe-Simon, Felisa; Elser, James J.
  • Limnology and Oceanography, Vol. 55, Issue 2
  • DOI: 10.4319/lo.2010.55.2.0667

Environmental Transcription of mmoX by Methane-Oxidizing Proteobacteria in a Subarctic Palsa Peatland
journal, October 2012

  • Liebner, Susanne; Svenning, Mette M.
  • Applied and Environmental Microbiology, Vol. 79, Issue 2
  • DOI: 10.1128/AEM.02292-12

Investigations of the structure and function of bacterial communities associated with Sphagnum mosses
journal, November 2007


Molybdenum and vanadium nitrogenases of Azotobacter chroococcum. Low temperature favours N2 reduction by vanadium nitrogenase
journal, December 1988

  • Miller, R. W.; Eady, R. R.
  • Biochemical Journal, Vol. 256, Issue 2
  • DOI: 10.1042/bj2560429

Alpha- and Gammaproteobacterial Methanotrophs Codominate the Active Methane-Oxidizing Communities in an Acidic Boreal Peat Bog
journal, February 2016

  • Esson, Kaitlin C.; Lin, Xueju; Kumaresan, Deepak
  • Applied and Environmental Microbiology, Vol. 82, Issue 8
  • DOI: 10.1128/AEM.03640-15

Effects of nitrogen fertilization on diazotrophic activity of microorganisms associated with Sphagnum magellanicum
journal, March 2016


Metal limitation of cyanobacterial N 2 fixation and implications for the Precambrian nitrogen cycle
journal, December 2006


Oxygen relations of nitrogen fixation in cyanobacteria.
journal, January 1992


Temperature-Dependent Regulation by Molybdenum and Vanadium of Expression of the Structural Genes Encoding Three Nitrogenases in Azotobacter vinelandii
journal, January 1991


Isolation of Nitrogen-Fixing Bacteria Containing Molybdenum-Independent Nitrogenases from Natural Environments
journal, September 1999


Acetylene reduction by pure cultures of Rhizobia.
journal, January 1975


Influence of Acetylene on Growth of Sulfate-Respiring Bacteria
journal, January 1982


The Nitrogen Cycle in Boreal Peatlands
book, January 2006


Oxygen requirement for acetylene reduction by pure cultures of rhizobia.
journal, January 1976


Peatland Biogeochemistry and Watershed Hydrology at the Marcell Experimental Forest
book, January 2011

  • Kolka, Randall; Sebestyen, Stephen; Verry, Elon S.
  • CRC Press
  • DOI: 10.1201/b10708

Works referencing / citing this record:

Vertical Variation of Nitrogen Fixers and Ammonia Oxidizers along a Sediment Profile in the Dajiuhu Peatland, Central China
journal, April 2019


Abundance and taxonomic affiliation of molybdenum transport and utilization genes in Tengchong hot springs, China
journal, May 2018

  • Srivastava, Shreya; Briggs, Brandon R.; Dong, Hailiang
  • Environmental Microbiology, Vol. 20, Issue 7
  • DOI: 10.1111/1462-2920.14250

Experimental warming alters the community composition, diversity, and N 2 fixation activity of peat moss ( Sphagnum fallax ) microbiomes
journal, May 2019

  • Carrell, Alyssa A.; Kolton, Max; Glass, Jennifer B.
  • Global Change Biology, Vol. 25, Issue 9
  • DOI: 10.1111/gcb.14715

Diazotroph Community Characterization via a High-Throughput nifH Amplicon Sequencing and Analysis Pipeline
journal, November 2017

  • Gaby, John Christian; Rishishwar, Lavanya; Valderrama-Aguirre, Lina C.
  • Applied and Environmental Microbiology, Vol. 84, Issue 4
  • DOI: 10.1128/aem.01512-17

The influence of oxygen and methane on nitrogen fixation in subarctic Sphagnum mosses
journal, May 2018