The hidden diversity and functional potential of Chloroflexota genomes in arsenic and antimony co-contaminated soils

Abstract

A total of 170 middle- and high-quality Chloroflexota MAGs were reconstructed from As and Sb co-contaminated soils. Many Chloroflexota MAGs have overlooked potential for C fixation and P solubilization. The enriched As, Sb, P, C and N metabolism genes in the MAGs favor Chloroflexota to resist contamination and nutrient limitations. Microorganisms were reported to be the indicators and drivers of metal(loid)s-contaminated soils. Chloroflexota is a widely-distributed phylum in arsenic (As) and antimony (Sb) contaminated soils, but the diversity and functional potential of its genomes remain largely unknown. In this study, we collected As and Sb contaminated soils from smelting-affected agricultural soils and mining soils, with the latter exhibiting much higher concentrations of As (mean 19421.2 mg kg−1) and Sb (mean 4953.5 mg kg−1) as well as lower carbon and nitrogen levels. We reconstructed 170 medium- to high-quality metagenome-assembled genomes (MAGs) of Chloroflexota from these soils. A total of 11 MAGs were proposed as novel candidate species, including 3 novel candidate genera affiliated with the classes Ktedonobacteria, Limnocylindria, and Dormibacteria. Functional annotation reveals that many MAGs from Ktedonobacteria and Dormibacteria may have novel potential for carbon fixation through the Calvin–Benson–Bassham cycle. Additionally, many Chloroflexota MAGs harbored essential genes involved in enhancing soil phosphorus (P) availability. In Chloroflexota MAGs, the gene responsible for extracellular oxidation, dldH, rather than the intracellular oxidation gene arsO, was widespread for Sb(III) oxidation. Under heavy As and Sb contamination and nutrient limitation, Chloroflexota MAGs exhibited higher guanine-cytosine contents and smaller genome sizes. Moreover, MAGs derived from these conditions were enriched with a higher proportion of genes related to Sb oxidation, As/P transport, As reduction and methylation, as well as pathways involved in carbohydrate degradation and bioavailable nitrogen biosynthesis. These findings might be helpful for developing bioremediation strategy for Chloroflexota in As/Sb contaminated soils. (Figure presented.)