Friends or foes? Virus-encoded auxiliary metabolism and pesticide degradation genes might promote bacterial survival in pesticide-contaminated soils

Viral auxiliary metabolic genes might help bacteria survive in pesticide-contaminated soils.
Friends or foes? Virus-encoded auxiliary metabolism and pesticide degradation genes might promote bacterial survival in pesticide-contaminated soils

Bacterial viruses, phages, are typically viewed as parasites that proliferate and kill their host via lysis. However, some phages can also peacefully live and propagate as integrated prophages in their host genomes in a lysogenic state. By doing so, they can contribute to bacterial fitness by carrying genes that are useful for the host, such as antibiotic resistance encoding genes. Accumulating evidence suggests that soil viruses also often carry auxiliary metabolic genes (AMGs) that can affect the host bacterial metabolism, potentially contributing to cycling of the elements and bacterial growth and survival. Even though viral AMGs are carried by phages, they are derived from other bacteria, and hence, phages act as agents for bacterial recombination via horizontal gene transfer. Here, we focused on characterizing the type of AMGs soil viruses carry in non-contaminated and contaminated soil microbiomes and asking if they might be beneficial for their host bacteria under environmental stress?

We specifically focused on soils contaminated by organochlorine pesticides (OCPs) (Fig. 1). OCPs are pesticides with vast applications in chemical and agricultural industries, imposing a serious threat to natural ecosystems and public health globally. Following the implementation of the Stockholm Convention, many pesticide factories in China were closed or re-located, but contaminated soils around the abandoned sites were left untreated. While OCPs can be toxic for soil microbial communities, some bacteria are able to break down these compounds. Hence, there is a growing interest in biotechnology to identify important genes underlying pesticide biodegradation. To study this, we focused on one OCP-contaminated site in the Yangtze River Delta region and characterized bacterial and phage metabolic and pesticide degradation associated genes using metagenomic sequencing (Fig. 1).

Figure 1. Aerial view of sampling site in Yangtze River Delta region. Non-contaminated area around the factory was used as a clean control soil.

We found that OCP-contaminated soils displayed a lower bacterial, but higher diversity of viruses. Moreover, around 14% of identified viruses in our data were novel and not previously characterized, and overall,  OCP-contaminated soils were associated with distinct bacterial and viral communities. The relatively higher diversity of viruses in the contaminated soil prompt a question: could viral taxonomic diversity be also linked with high functional gene diversity in the contaminated soil? The answer is yes viruses recovered from OCP-contaminated soil harbored a higher relative abundance of AMGs linked to pesticide degradation and metabolism. Furthermore, the diversity and relative abundance of AMGs significantly increased along with the severity of pesticide contamination, and several biodegradation genes were identified in viral metagenomes after careful bioinformatic analysis and manual curation(Fig. 2). These findings suggest that viruses could potentially help their bacterial hosts to survive in contaminated soils by providing important genes for OCP degradation.

Figure 2. Relative abundances and number of bacterial and virus-encoded genes in clean and OCP-contaminated soils.

To test this idea experimentally, we focused on the virus-encoded L-2-Haloacid dehalogenase gene (L-DEX), which catalyzes the hydrolytic dehalogenation of L-2-haloacids important precursors for the synthesis of pesticides, including Hexachlorocyclohexane, which is a persistent organochlorine insecticide. In addition, one of its substrates, 2-chloropropionic acid, is also a commonly used broad-spectrum herbicide. The degradation activity of the purified, virus-encoded L-DEX protein was investigated experimentally (Fig. 3). It was found that L-DEX could break down two haloacid precursors, monochloroacetate (MCA) and S(L)-2-chloropropionic acid (S-2-CPA), leading to detoxification of the environment. Moreover, the presence of L-DEX plasmid allowed E. coli host bacterium to grow better at subinhibitory S-2-CPA concentrations. Together, these results show that virus-encoded L-DEX formed an active protein that was beneficial for the host bacterium by breaking down pesticides and improving its growth.

Figure 3.  Experimental functional validation of virus-encoded pesticide degradation L-DEX gene.

 The results are exciting because they not only provide an ecological insight into the interaction between viruses and their host bacteria in stressful environments but also suggest that perhaps it is possible to use phages for bioremediation of contaminated soils in the future. It would also be interesting to study if identified phage-encoded degradation genes have evolved only recently due to human pesticide manufacturing or if they have a more distant evolutionary origin.

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