Genetic and phylogenetic analysis of dissimilatory iodate-reducing bacteria identifies potential niches across the world’s oceans

Abstract

Iodine is oxidized and reduced as part of a biogeochemical cycle that is especially pronounced in the oceans, where the element naturally concentrates. The use of oxidized iodine in the form of iodate (IO3−) as an electron acceptor by microorganisms is poorly understood. Here, we outline genetic, physiological, and ecological models for dissimilatory IO3− reduction to iodide (I−) by a novel estuarine bacterium, Denitromonas sp. IR-12. Our results show that dissimilatory iodate reduction (DIR) by strain IR-12 is molybdenum-dependent and requires an IO3− reductase (idrA) and likely other genes in a mobile cluster with a conserved association across known and predicted DIR microorganisms (DIRM). Based on genetic and physiological data, we propose a model where three molecules of IO3− are likely reduced to three molecules of hypoiodous acid (HIO), which rapidly disproportionate into one molecule of IO3− and two molecules of iodide (I−), in a respiratory pathway that provides an energy yield equivalent to that of nitrate or perchlorate respiration. Consistent with the ecological niche expected of such a metabolism, idrA is enriched in the metagenome sequence databases of marine sites with a specific biogeochemical signature (high concentrations of nitrate and phosphate) and diminished oxygen. Taken together, these data suggest that DIRM help explain the disequilibrium of the IO3−:I− concentration ratio above oxygen-minimum zones and support a widespread iodine redox cycle mediated by microbiology.

Isolation of a Dissimilatory Iodate-Reducing Aromatoleum sp. From a Freshwater Creek in the San Francisco Bay Area

“…TC-10 and the previously described DIRM Denitromonas sp. IR-12 ( Reyes-Umana et al, 2021 ). In A. toluclasticum , 52% of the total carbon is assimilated into biomass, whereas Denitromonas sp.…”

“…The physiochemical state of water suggests that iodine is most stable as IO 3 – , yet I – predominates across many regions of high biological productivity globally ( Luther et al, 1995 ; Gonzales et al, 2017 ). Recent work suggests that a diverse group of dissimilatory iodate reducing microorganisms (DIRM) consisting mainly of marine Proteobacteria may contribute to this phenomenon in oceanic environments ( Reyes-Umana et al, 2021 ). Metagenomic surveys indicate that DIRM are ubiquitous in the Earth’s oceans and are associated with marine life or live above oxygen minimum zones ( Reyes-Umana et al, 2021 ).…”

“…Recent work suggests that a diverse group of dissimilatory iodate reducing microorganisms (DIRM) consisting mainly of marine Proteobacteria may contribute to this phenomenon in oceanic environments ( Reyes-Umana et al, 2021 ). Metagenomic surveys indicate that DIRM are ubiquitous in the Earth’s oceans and are associated with marine life or live above oxygen minimum zones ( Reyes-Umana et al, 2021 ). DIRM are defined characteristically by the ability to reduce relatively high concentrations of iodate (IO 3 – ) to iodide (I – ) and couple it to growth.…”

“…DIRM are defined characteristically by the ability to reduce relatively high concentrations of iodate (IO 3 – ) to iodide (I – ) and couple it to growth. Dissimilatory iodate respiration (DIR) is dependent on a dedicated iodate reduction genomic island (IRI) that is horizontally transferred between diverse taxa ( Reyes-Umana et al, 2021 ). The IRI is composed of a heterodimeric iodate reductase (IdrAB), and two distinct putative cytochrome c peroxidases (IdrP1 and IdrP2).…”

“…The IRI is composed of a heterodimeric iodate reductase (IdrAB), and two distinct putative cytochrome c peroxidases (IdrP1 and IdrP2). The IdrA is a highly conserved molybdenum-dependent member of the DMSO reductase protein superfamily closely related to dissimilatory nitrate reductases and perchlorate reductases ( Reyes-Umana et al, 2021 ).…”