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.

Keywords: Marcell Experimental Forest; SPRUCE; carbon cycling; metagenomics; microbial community; microbiome; nitrogen cycling; organic nitrogen; soil carbon; soil organic matter.