Molybdenum-Based Diazotrophy in a Sphagnum Peatland in Northern Minnesota

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.

doi:10.1128/AEM.01174-17

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

Journal Article · Fri Jun 30 00:00:00 EDT 2017 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/AEM.01174-17· OSTI ID:1394354

Warren, Melissa J. ^[1]; Lin, Xueju ^[2]; Gaby, John C. ^[2]; Kretz, Cecilia B. ^[1]; Kolton, Max ^[2]; Morton, Peter L. ^[3]; Pett-Ridge, Jennifer ^[4]; Weston, David J. ^[5]; Schadt, Christopher W. ^[5]; Kostka, Joel E. ^[6];

^[6]

Georgia Inst. of Technology, Atlanta, GA (United States). School of Earth and Atmospheric Sciences
Georgia Inst. of Technology, Atlanta, GA (United States). School of Biological Sciences
Florida State Univ., Tallahassee, FL (United States). National High Magnetic Field Lab. (MagLab)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Physical and Life Sciences Directorate
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Divison
Georgia Inst. of Technology, Atlanta, GA (United States). School of Earth and Atmospheric Sciences and School of Biological Sciences

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.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC05-00OR22725; SC0007144; SC0012088; AC52-07NA27344

OSTI ID:: 1394354

Alternate ID(s):: OSTI ID: 1478664

Report Number(s):: LLNL-JRNL-731618

Journal Information:: Applied and Environmental Microbiology, Vol. 83, Issue 17; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 39 works

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Effects of nitrogen fertilization on diazotrophic activity of microorganisms associated with Sphagnum magellanicum Kox, Martine A. R.; Lüke, Claudia; Fritz, Christian Plant and Soil, Vol. 406, Issue 1-2 https://doi.org/10.1007/s11104-016-2851-z	journal	March 2016
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Temperature-Dependent Regulation by Molybdenum and Vanadium of Expression of the Structural Genes Encoding Three Nitrogenases in Azotobacter vinelandii Walmsley, Jean; Kennedy, Christina Applied and Environmental Microbiology, Vol. 57, Issue 2 https://doi.org/10.1128/AEM.57.2.622-624.1991	journal	January 1991
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Succession of microbial populations and nitrogen-fixation associated with the biodegradation of sediment-oil-agglomerates buried in a Florida sandy beach Shin, Boryoung; Bociu, Ioana; Kolton, Max Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-55625-6	journal	December 2019
Abundance and taxonomic affiliation of molybdenum transport and utilization genes in Tengchong hot springs, China Srivastava, Shreya; Briggs, Brandon R.; Dong, Hailiang Environmental Microbiology, Vol. 20, Issue 7 https://doi.org/10.1111/1462-2920.14250	journal	May 2018
Experimental warming alters the community composition, diversity, and N ₂ fixation activity of peat moss ( Sphagnum fallax ) microbiomes Carrell, Alyssa A.; Kolton, Max; Glass, Jennifer B. Global Change Biology, Vol. 25, Issue 9 https://doi.org/10.1111/gcb.14715	journal	May 2019
Diazotroph Community Characterization via a High-Throughput nifH Amplicon Sequencing and Analysis Pipeline Gaby, John Christian; Rishishwar, Lavanya; Valderrama-Aguirre, Lina C. Applied and Environmental Microbiology, Vol. 84, Issue 4 https://doi.org/10.1128/aem.01512-17	journal	November 2017
The influence of oxygen and methane on nitrogen fixation in subarctic Sphagnum mosses Kox, Martine A. R.; Aalto, Sanni L.; Penttilä, Timo AMB Express, Vol. 8, Issue 1 https://doi.org/10.1186/s13568-018-0607-2	journal	May 2018

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59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Alphaproteobacteria
Sphagnum
acetylene
diazotrophy
methanotrophs
molybdenum
nitrogen cycle enzymes
nitrogen fixation
peatland
vanadium

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