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High Genetic Potential for Proteolytic Decomposition in Northern Peatland Ecosystems.

ABSTRACT: Nitrogen (N) is a scarce nutrient commonly limiting primary productivity. Microbial decomposition of complex carbon (C) into small organic molecules (e.g., free amino acids) has been suggested to supplement biologically fixed N in northern peatlands. We evaluated the microbial (fungal, bacterial, and archaeal) genetic potential for organic N depolymerization in peatlands at Marcell Experimental Forest (MEF) in northern Minnesota. We used guided gene assembly to examine the abundance and diversity of protease genes and further compared them to those of N fixation (nifH) genes in shotgun metagenomic data collected across depths and in two distinct peatland environments (bogs and fens). Microbial protease genes greatly outnumbered nifH genes, with the most abundant genes (archaeal M1 and bacterial trypsin [S01]) each containing more sequences than all sequences attributed to nifH Bacterial protease gene assemblies were diverse and abundant across depth profiles, indicating a role for bacteria in releasing free amino acids from peptides through depolymerization of older organic material and contrasting with the paradigm of fungal dominance in depolymerization in forest soils. Although protease gene assemblies for fungi were much less abundant overall than those for bacteria, fungi were prevalent in surface samples and therefore may be vital in degrading large soil polymers from fresh plant inputs during the early stage of depolymerization. In total, we demonstrate that depolymerization enzymes from a diverse suite of microorganisms, including understudied bacterial and archaeal lineages, are prevalent within northern peatlands and likely to influence C and N cycling.IMPORTANCE Nitrogen (N) is a common limitation on primary productivity, and its source remains unresolved in northern peatlands that are vulnerable to environmental change. Decomposition of complex organic matter into free amino acids has been proposed as an important N source, but the genetic potential of microorganisms mediating this process has not been examined. Such information can inform possible responses of northern peatlands to environmental change. We show high genetic potential for microbial production of free amino acids across a range of microbial guilds in northern peatlands. In particular, the abundance and diversity of bacterial genes encoding proteolytic activity suggest a predominant role for bacteria in regulating productivity and contrasts with a paradigm of fungal dominance of organic N decomposition. Our results expand our current understanding of coupled carbon and nitrogen cycles in northern peatlands and indicate that understudied bacterial and archaeal lineages may be central in this ecosystem's response to environmental change.

SUBMITTER: Graham EB

PROVIDER: S-EPMC6498154 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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High Genetic Potential for Proteolytic Decomposition in Northern Peatland Ecosystems.

Graham Emily B EB Yang Fan F Bell Sheryl S Hofmockel Kirsten S KS

Applied and environmental microbiology 20190502 10

Nitrogen (N) is a scarce nutrient commonly limiting primary productivity. Microbial decomposition of complex carbon (C) into small organic molecules (e.g., free amino acids) has been suggested to supplement biologically fixed N in northern peatlands. We evaluated the microbial (fungal, bacterial, and archaeal) genetic potential for organic N depolymerization in peatlands at Marcell Experimental Forest (MEF) in northern Minnesota. We used guided gene assembly to examine the abundance and diversit ...[more]

PMID: 30850433

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Project description:Microbial N2 fixation (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 ombrotrophic Sphagnum-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 and 15N2 incorporation. A molecular analysis of metabolically active microbial communities suggested that diazotrophy in surface peat was primarily mediated by Alphaproteobacteria (Bradyrhizobiaceae and Beijerinckiaceae). 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 of 15N2 was suppressed 90% by O2 and 55% by C2H2 and was unaffected by CH4 and CO2 amendments. 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 O2 and 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 in Sphagnum-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 the Alphaproteobacteria (Rhizobiales) catalyze this process at the bog surface using the molybdenum-based form of the nitrogenase enzyme.

Project description:Differences in litter quality, microbial activity or abiotic conditions cannot fully account for the variability in decomposition rates observed in semiarid ecosystems. Here we tested the role of variation in litter quality, water supply, and UV radiation as drivers of litter decomposition in arid lands. And show that carry-over effects of litter photodegradation during dry periods can regulate decomposition during subsequent wet periods. We present data from a two-phase experiment, where we first exposed litter from a drought-deciduous and an evergreen shrub to natural UV levels during five, rainless summer months and, subsequently, in the laboratory, we assessed the carry-over effects of photodegradation on biomass loss under different irrigation treatments representing the observed range of local rainfall variation among years (15-240 mm). Photodegradation of litter in the field produced average carbon losses of 12%, but deciduous Proustia pungens lost >25%, while evergreen Porlieria chilensis less than 5%. Natural exposure to UV significantly reduced carbon-to-nitrogen and lignin:N ratios in Proustia litter but not in Porlieria. During the subsequent wet phase, remaining litter biomass was lower in Proustia than in Porlieria. Indeed UV exposure increased litter decomposition of Proustia under low and medium rainfall treatments, whereas no carry-over effects were detected under high rainfall treatment. Consequently, for deciduous Proustia carry-over effects of UV exposure were negligible under high irrigation. Litter decomposition of the evergreen Porlieria depended solely on levels of rainfall that promote microbial decomposers. Our two-phase experiment revealed that both the carry-over effects of photodegradation and litter quality, modulated by inter-annual variability in rainfall, can explain the marked differences in decomposition rates and the frequent decoupling between rainfall and litter decomposition observed in semiarid ecosystems.

Dataset Information

High Genetic Potential for Proteolytic Decomposition in Northern Peatland Ecosystems.

Publications

High Genetic Potential for Proteolytic Decomposition in Northern Peatland Ecosystems.

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