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

www.nature.com/ismej ARTICLE OPEN Genetic and phylogenetic analysis of dissimilatory iodatereducing bacteria identifies potential niches across the world’s oceans Victor Reyes-Umana 1 , Zachary Henning1, Kristina Lee1, Tyler P. Barnum1 and John D. Coates 1✉ © The Author(s) 2021 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. The ISME Journal; https://doi.org/10.1038/s41396-021-01034-5 INTRODUCTION Iodine (as 127I) is the heaviest stable element of biological importance and an essential component of the human diet due to its role in thyroxine biosynthesis in vertebrates [1–3]. Iodine is enriched in marine environments where it exists in several oxidation states, reaching concentrations of up to 450 nM [4]. In these environments, organisms such as kelp bioconcentrate iodine as iodide (I−) and produce volatile iodine species such as methyl iodide [5]. These volatile iodine species contribute to the destruction of tropospheric ozone (a major greenhouse gas) and aerosol formation at the marine boundary layer, consequently resulting in cloud formation and other local climatic effects [1, 6]. Despite the global biological and geochemical importance of iodine, little is known about its biogeochemistry in the ocean [4]. For instance, the biological mechanism accounting for the unexpected chemical disequilibrium between I− and iodate (IO3−) in seawater (I−:IO3− disequilibrium) remains unknown [4]. At the physicochemical conditions of seawater, iodine is most stable as IO3− [7], yet measurements of IO3− and I− in regions with high biological productivity (e.g., marine photic zones, kelp forests, or sediments), reveal an enrichment of the I− ion beyond what can be explained through abiotic reduction [7, 8] with ferrous iron [9] or sulfide. Among numerous explanations proposed for I− enrichment, microbial IO3− reduction is particularly compelling. The high reduction potential (IO3−/I− Eh = 0.72 V at pH 8.1) [7, 10] makes IO3− an ideal electron acceptor for microbial metabolism in marine environments. Early studies indicated common microorganisms such as Escherichia coli and Shewanella putrefaciens, reduce IO3− to I− [10, 11]. Subsequent studies associated this metabolism with the inadvertent activity of DMSO respiratory reductase enzymes in marine environments, along with specific enzymes (i.e., perchlorate reductase, nitrate reductase) that reduce IO3− in vitro [10, 12, 13]. However, there is little evidence that organisms hosting these enzymes are capable of growth by IO3− reduction. While inadvertent IO3- reduction might be mediated by marine bacteria possessing DMSO reductases, until recently, no definitive evidence existed that global IO3− reduction is a microbially assisted phenomenon. In support of a microbial role for the observed I−:IO3− disequilibrium, previous studies demonstrated that at least one member each of the common marine genera Pseudomonas and Shewanella are capable of IO3− reduction [13–15]. More recently, IO3− reduction by Pseudomonas sp. strain SCT was associated with a molybdopterin oxidoreductase closely related to arsenite oxidase [15]. As part of this work, a dedicated biochemical pathway was proposed involving two peroxidases associated with a heterodimeric IO3− reductase (Idr) [15]. The putative model proposes a four-electron transfer mediated by Idr, resulting in the production of hydrogen peroxide and hypoiodous acid [15]. Two peroxidases detoxify the hydrogen peroxide while a chlorite dismutase (Cld) homolog dismutates the Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA. ✉email: 1 Received: 11 December 2020 Revised: 27 May 2021 Accepted: 3 June 2021 V. Reyes-Umana et al. 1234567890();,: 2 Fig. 1 Phylogeny and physiology of Denitromonas sp. IR-12. A 16S rRNA gene phylogeny of Denitromonas sp. IR-12 (denoted by a purple star) belonging to a subclade of Azoarcus, separate from other known Azoarcus species. B TEM images of an active culture of Denitromonas sp. IR-12 with the scale at 2 μm (left) and 0.2 μm (right) taken on a Technai 12 TEM. C Iodate consumption across all five conditions assessed in the growth experiment in D. N = 3 and error bars show standard deviation. D Iodate consumption ( ), acetate consumption ( ), iodide production ( ), and growth ( ; measured as optical density at λ=600 nm; OD600) in an active culture of Denitromonas sp. IR-12 growing anaerobically. N = 3 and error bars show standard deviation. E Optical density (OD600) in the presence ( ), absence ( ), and amendment of MoO42- after 14 hours incubation ( ). N = 7 and error bars show standard deviation. hypoiodous acid into I− and molecular oxygen, which is subsequently reduced by the organism [15]. The proposed pathway involving a molecular O2 intermediate is analogous to canonical microbial perchlorate respiration [16]. By contrast, Toporek et al. [17]. using the IO3− respiring Shewanella oneidensis demonstrated the involvement of an unidentified reductase associated with the mtrAB multiheme cytochrome, suggesting an alternative dissimilatory iodate reduction (DIR) pathway. The disparate mechanisms underscore the potential diversity of IO3− respiratory processes. As such, identification of additional DIR microorganisms (DIRM) would clarify which genes are required for this metabolism and enable identification of IO3− respiratory genes in metagenomes. With this as a primary objective, we identified a novel marine DIRM, Denitromonas sp. strain IR-12, that obtained energy for growth by cou (...truncated)