Differential Responses of Dinitrogen Fixation, Diazotrophic Cyanobacteria and Ammonia Oxidation Reveal a Potential Warming-Induced Imbalance of the N-Cycle in Biological Soil Crusts.

Xiaobing Zhou,Hilda Smith,Ana Giraldo Silva,Ferran Garcia-Pichel,Jayne Belnap,Daniele Daffonchio

doi:10.1371/journal.pone.0164932

Abstract

N2 fixation and ammonia oxidation (AO) are the two most important processes in the nitrogen (N) cycle of biological soil crusts (BSCs). We studied the short-term response of acetylene reduction assay (ARA) rates, an indicator of potential N2 fixation, and AO rates to temperature (T, -5°C to 35°C) in BSC of different successional stages along the BSC ecological succession and geographic origin (hot Chihuahuan and cooler Great Basin deserts). ARA in all BSCs increased with T until saturation occurred between 15 and 20°C, and declined at 30–35°C. Culture studies using cyanobacteria isolated from these crusts indicated that the saturating effect was traceable to their inability to grow well diazotrophically within the high temperature range. Below saturation, temperature response was exponential, with Q10 significantly different in the two areas (~ 5 for Great Basin BSCs; 2–3 for Chihuahuan BSCs), but similar between the two successional stages. However, in contrast to ARA, AO showed a steady increase to 30–35°C in Great Basin, and Chihuhuan BSCs showed no inhibition at any tested temperature. The T response of AO also differed significantly between Great Basin (Q10 of 4.5–4.8) and Chihuahuan (Q10 of 2.4–2.6) BSCs, but not between successional stages. Response of ARA rates to T did not differ from that of AO in either desert. Thus, while both processes scaled to T in unison until 20°C, they separated to an increasing degree at higher temperature. As future warming is likely to occur in the regions where BSCs are often the dominant living cover, this predicted decoupling is expected to result in higher proportion of nitrates in soil relative to ammonium. As nitrate is more easily lost as leachate or to be reduced to gaseous forms, this could mean a depletion of soil N over large landscapes globally.

Highlights

Biological soil crusts (BSCs) are complex soil surface communities with cyanobacteria, green algae, lichens or mosses as primary producers [1]
Differences in BSC successional stage were reflected in the proxy of phototrophic biomass, which for a given locality were lower in light than in dark/lichen BSCs
More mature BSCs had a higher concentration of scytonemin, reflective of larger numbers of heterocystous cyanobacteria [45]

Summary

Introduction

Biological soil crusts (BSCs) are complex soil surface communities with cyanobacteria, green algae, lichens or mosses as primary producers [1]. They contain significant populations of heterotrophic bacteria, archaea [2] and fungi [3], as well as chemolithotrophic microbes [4]. They are common in dryland regions, where they can reach up to 70% of the living cover [5], and are an important element of these ecosystems both locally and globally [6]. They stabilize the soil surface [9, 10], fix atmospheric carbon (C) and N [8, 11,12,13,14,15], alter the soil content of many metals and metalloids [16], may help maintain vascular plant diversity [17, 18], and affect hydrological processes [19,20,21]

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Discussion

Conclusion