Shifts in Soil Structure, Biological, and Functional Diversity Under Long-Term Carbon Deprivation.

Paul B L George,James E Mcdonald,Simon Creer,David B Fidler,David A Robinson,Davey L Jones,Joy D Van Nostrand,Sacha J Mooney,Robert I Griffiths,Jonathan A Atkinson

doi:10.3389/fmicb.2021.735022

Abstract

Soil organic matter is composed of a variety of carbon (C) forms. However, not all forms are equally accessible to soil microorganisms. Deprivation of C inputs will cause changes in the physical and microbial community structures of soils; yet the trajectories of such changes are not clear. We assessed microbial communities using phospholipid fatty acid profiling, metabarcoding, CO2 emissions, and functional gene microarrays in a decade-long C deprivation field experiment. We also assessed changes in a range of soil physicochemical properties, including using X-ray Computed Tomography imaging to assess differences in soil structure. Two sets of soils were deprived of C inputs by removing plant inputs for 10 years and 1 year, respectively. We found a reduction in diversity measures, after 10 years of C deprivation, which was unexpected based on previous research. Fungi appeared to be most impacted, likely due to competition for scarce resources after exhausting the available plant material. This suggestion was supported by evidence of bioindicator taxa in non-vegetated soils that may directly compete with or consume fungi. There was also a reduction in copies of most functional genes after 10 years of C deprivation, though gene copies increased for phytase and some genes involved in decomposing recalcitrant C and methanogenesis. Additionally, soils under C deprivation displayed expected reductions in pH, organic C, nitrogen, and biomass as well as reduced mean pore size, especially in larger pores. However, pore connectivity increased after 10 years of C deprivation contrary to expectations. Our results highlight concurrent collapse of soil structure and biodiversity following long-term C deprivation. Overall, this study shows the negative trajectory of continuous C deprivation and loss of organic matter on a wide range of soil quality indicators and microorganisms.

Highlights

Soil carbon (C) loss is a serious concern for global agricultural management in addition to contributing to climate change (Lal, 2004)
Concentrations of all cations, except Al and Mg, and Cation exchange capacity (CEC) as well as soil CO2 flux were significantly greater in vegetated soils
We have shown that C deprivation of only a decade can reduce soil biodiversity measures, in contrast to previous work that found more resilience in the microbial community

Summary

Introduction

Soil carbon (C) loss is a serious concern for global agricultural management in addition to contributing to climate change (Lal, 2004). Bellamy et al (2005) reported that organic C is lost from soils in England and Wales at a rate of 0.6% per year; UKCEH-Countryside Survey support the loss in agricultural soils (Reynolds et al, 2013), but is yet to find evidence in other habitats. More recalcitrant C forms, such as lignin and high molecular weight, complex humic substances reside much longer in soils (Rovira and Vallejo, 2002; Romero-Olivares et al, 2017; Lehmann et al, 2020), and are thought to be decomposed primarily by fungi (Adl, 2003), though recent evidence suggests that saprotrophic fungi are more prominent consumers of labile C than previously understood (de Vries and Caruso, 2016). As labile and exposed soil C sources are depleted, it is expected that organisms capable of exploiting recalcitrant C forms are more likely to persist

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