Metagenomic Insights into Anaerobic Metabolism along an Arctic Peat Soil Profile

David A Lipson,Shashank Sathe,John Matthew Haggerty,Archana Srinivas,Elizabeth A Dinsdale,Theodore K Raab,Zhi Zhou

doi:10.1371/journal.pone.0064659

David A Lipson, Shashank Sathe + Show 5 more

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https://doi.org/10.1371/journal.pone.0064659

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Abstract

A metagenomic analysis was performed on a soil profile from a wet tundra site in northern Alaska. The goal was to link existing biogeochemical knowledge of the system with the organisms and genes responsible for the relevant metabolic pathways. We specifically investigated how the importance of iron (Fe) oxides and humic substances (HS) as terminal electron acceptors in this ecosystem is expressed genetically, and how respiratory and fermentative processes varied with soil depth into the active layer and into the upper permafrost. Overall, the metagenomes reflected a microbial community enriched in a diverse range of anaerobic pathways, with a preponderance of known Fe reducing species at all depths in the profile. The abundance of sequences associated with anaerobic metabolic processes generally increased with depth, while aerobic cytochrome c oxidases decreased. Methanogenesis genes and methanogen genomes followed the pattern of CH4 fluxes : they increased steeply with depth into the active layer, but declined somewhat over the transition zone between the lower active layer and the upper permafrost. The latter was relatively enriched in fermentative and anaerobic respiratory pathways. A survey of decaheme cytochromes (MtrA, MtrC and their homologs) revealed that this is a promising approach to identifying potential reducers of Fe(III) or HS, and indicated a possible role for Acidobacteria as Fe reducers in these soils. Methanogens appear to coexist in the same layers, though in lower abundance, with Fe reducing bacteria and other potential competitors, including acetogens. These observations provide a rich set of hypotheses for further targeted study.

Highlights

Given the large carbon (C) pools in permafrost-affected soils and the rapid rates of climate warming at high latitudes [1,2], an improved understanding of metabolic processes in Arctic soils would be valuable [3]
Given the importance of the water table, oxygen concentration and redox state in controlling biogeochemistry in these soils [8], how does the relative abundance of respiratory and fermentative pathways change with depth in the active layer and into the upper level of the permafrost? The presence of Fe(III) and other alternative electron acceptors is generally inhibitory to methanogens [15] and the two processes appear to be negatively correlated at our site [8], but it is not known to what extent methanogens coexist spatially with Fe reducers in these soils or whether they are segregated by depth
Extractable Fe minerals were generally higher in the mineral horizon, but both substrates and products of Fe reduction were abundant at all depths (Table 1)

Summary

Introduction

Given the large carbon (C) pools in permafrost-affected soils and the rapid rates of climate warming at high latitudes [1,2], an improved understanding of metabolic processes in Arctic soils would be valuable [3]. Our acidic wet tundra site in the Arctic coastal plain of northern Alaska contrasts with each of these sites, and may be unique in that anaerobic respiration using Fe(III) and/or humic substances (HS) as terminal electron acceptor contributes greatly to C cycling in this soil [7,8,9]. Because these electron acceptors are generally complex and insoluble, these processes occur through extracellular electron transport via outer membrane cytochromes [10]. In this study we focus on anaerobic metabolism as revealed by metagenomic analysis of an Arctic peat soil profile that spans the active layer (0–30 cm in 10 cm increments) and the upper permafrost (30–40 cm)

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