Abstract

Chemical contamination of natural and agricultural habitats is an increasing global problem and a major threat to sustainability and human health. Organophosphorus (OP) compounds are one major class of contaminant and can undergo microbial degradation, however, no studies have applied system-wide ecogenomic tools to investigate OP degradation or use metagenomics to understand the underlying mechanisms of biodegradation in situ and predict degradation potential. Thus, there is a lack of knowledge regarding the functional genes and genomic potential underpinning degradation and community responses to contamination. Here we address this knowledge gap by performing shotgun sequencing of community DNA from agricultural soils with a history of pesticide usage and profiling shifts in functional genes and microbial taxa abundance. Our results showed two distinct groups of soils defined by differing functional and taxonomic profiles. Degradation assays suggested that these groups corresponded to the organophosphorus degradation potential of soils, with the fastest degrading community being defined by increases in transport and nutrient cycling pathways and enzymes potentially involved in phosphorus metabolism. This was against a backdrop of taxonomic community shifts potentially related to contamination adaptation and reflecting the legacy of exposure. Overall our results highlight the value of using holistic system-wide metagenomic approaches as a tool to predict microbial degradation in the context of the ecology of contaminated habitats.

Highlights

  • Environmental contamination by toxic compounds has emerged as a major threat to environmental and human health globally (Singh and Naidu, 2012)

  • To determine the influence of the different legacy of pesticide exposure on contemporary microbial composition and to predict degradation potential, we profiled the metagenomic potential of the soils from these sites

  • Whilst many studies have analyzed individual catabolic genes involved in degradation of contaminants including pesticides (Li et al, 2008; Singh, 2009; Imfeld and Vuilleumier, 2012), and have applied metagenomics to assess the influence of contamination on functional potential (Hemme et al, 2010; Mason et al, 2012; Smith et al, 2013), this is the first study to use metagenomics to demonstrate that system-wide responses in the context of the degradation potential of the soils demonstrated experimentally

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Summary

Introduction

Environmental contamination by toxic compounds has emerged as a major threat to environmental and human health globally (Singh and Naidu, 2012). Large-scale chemical contamination has been identified as a “planetary boundary” alongside climate change, ocean acidification, eutrophication, species loss and shifts in nutrient cycling (Rockström et al, 2009). Efforts to address this problem, and remediate contaminated sites using the metabolic activities of microbes and plants to degrade contaminants in situ (Bioremediation), have been hampered by the lack of a holistic system-wide understanding of the complex interactions between degrading organisms and genes, the wider metabolic network of the microbial community, and the environmental variability in each specific habitat (de Lorenzo, 2008). There is a need to understand the relationship between microbial community composition and degradation potential and to elucidate which chemical variables and microbial diversity metrics can predict chemical degradation

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