Aridity Structures the Microbial Potential for Carbon Cycling and Mediates the Impact of Mammal Bioturbation at the Continental Scale

Abstract

Introduction

In Australia, the historical loss of native digging mammals has profoundly changed ecosystems and their functioning. However, little is known about how the decline in digging mammal presence alters microbes and their functional potential and how aridity affects these relationships.

Materials and Methods

We used metagenomic sequencing to explore changes in genes encoding enzymes for carbon cycling (CAZymes) in five sites along a continent-wide aridity gradient, with and without digging mammals.

Results

The diversity of CAZy genes was reduced with increases in aridity, which also affected their structure and reduced the abundance of genes involved in both plant (cellulose and starch) and microbial (glucans, peptidoglycan and chitin) biomass degradation. Conversely, digging mammals had a limited effect on the structure and diversity of CAZy genes, indicating an overall resistance of the microbial carbon cycling potential to mammal disturbance at the whole community level. However, when considering individual functional groups, digging activity increased the abundance of genes involved in microbial biomass decomposition (i.e., glucanases), while reducing the abundance of genes associated with recalcitrant plant biomass degradation (i.e., cellulases). Notably, these effects were observed only in the most arid sites and was mostly mediated by increases in SOM content linked to mammal activity.

Conclusions

Overall, our study shows that aridity shapes the diversity and structure of CAZy genes, while also modulating the effect of mammal bioturbation on the microbial potential for carbon cycling. This suggests that the loss of digging mammals throughout much of Australia's arid zone, in particular, is likely to have important repercussions on the microbial capacity to carry decomposition processes and the turnover of organic matter in soils.