Meta-omics-aided isolation of an elusive anaerobic arsenic-methylating soil bacterium

Abstract

Soil microbiomes harbour unparalleled functional and phylogenetic diversity. However, extracting isolates with a targeted function from complex microbiomes is not straightforward, particularly if the associated phenotype does not lend itself to high-throughput screening. Here, we tackle the methylation of arsenic (As) in anoxic soils. As methylation was proposed to be catalysed by sulfate-reducing bacteria. However, to date, there are no available anaerobic isolates capable of As methylation, whether sulfate-reducing or otherwise. The isolation of such a microorganism has been thwarted by the fact that the anaerobic bacteria harbouring a functional arsenite S-adenosylmethionine methyltransferase (ArsM) tested to date did not methylate As in pure culture. Additionally, fortuitous As methylation can result from the release of non-specific methyltransferases upon lysis. Thus, we combined metagenomics, metatranscriptomics, and metaproteomics to identify the microorganisms actively methylating As in anoxic soil-derived microbial cultures. Based on the metagenome-assembled genomes of microorganisms expressing ArsM, we isolated Paraclostridium sp. strain EML, which was confirmed to actively methylate As anaerobically. This work is an example of the application of meta-omics to the isolation of elusive microorganisms.

Genome-Resolved Metagenomics and Metatranscriptomics Reveal that Aquificae Dominates Arsenate Reduction in Tengchong Geothermal Springs

“…For example, in the cultures amended with As, Deltaproteobacteria populations did not transcribe arsM, although they contributed most of the arsM sequences. 70 Our study identified, for the first time, the considerable abundance and active expression of arsC in phylum Aquificae.…”

Methanogens-Driven Arsenic Methylation Preceding Formation of Methylated Thioarsenates in Sulfide-Rich Hot Springs

“…Some anaerobic microorganisms are thought to produce a toxic trivalent MMA(III) to kill their competitors, 78 which was hypothesized to promote arsenic methylation in a microbial community. 50 Indeed, cells expressed with arsM usually conveyed some level of resistance to MMA(III) 79 and so did arsenic-methylating microorganisms. 31 Besides, M. thermophila contains the arsR gene (Figure S16a), which is autoregulated and is typically part of an operon that contains other ars genes involved in arsenic detoxification.…”

“…BXM 49 and Paraclostridium sp. strain EML, 50 and ArsM enzymes purified from Desulfosporosinus meridiei and Desulfotonmaculum gibsoniae 14 were able to efficiently methylate arsenite. Two pure methanogens have been investigated for arsenic methylation as well, i.e., Methanosarcina mazei (M. mazei) Go1 40,51 and Methanosarcina acetivorans (M. acetivorans) C2A.…”

The need for an integrated multi‐OMICs approach in microbiome science in the food system

“…Similarly, the application of combined metagenomics, metatranscriptomics, and metaproteomics enabled the identification of the microorganisms actively methylating arsenic in anoxic soil-derived microbial cultures (Viacava et al, 2022). Furthermore, based on the analysis of the metagenome-assembled genomes of microorganisms expressing arsenite S-adenosylmethionine methyltransferase (ArsM), a targeted cultivation strategy was developed, resulting in the isolation of the Paraclostridium sp.…”