Introduction
As a trace element, iodine (I) plays a crucial role in human health as well as is of environmental significance. Iodine is a major component of the human thyroid hormones thyroxine (T4) and triiodothyronine (T3). Thus, iodine is an integrated part of the thyroid functions of humans and other vertebrates (Zimmermann, Reference Zimmermann2009). It has been estimated that iodine-deficient disorder (IDD) affects ~1.9 billion people worldwide, whose symptoms included thyroid enlargement (goiter) and cretinism (Santos et al., Reference Santos, Christoforou, Trieu, McKenzie, Downs, Billot, Webster and Li2019). Salt iodization and the fortification of foods, beverages and seasoning with iodine could efficiently prevent and control human IDD (Santos et al., Reference Santos, Christoforou, Trieu, McKenzie, Downs, Billot, Webster and Li2019; Zimmermann, Reference Zimmermann2009). Iodine supplementation in the human diet, however, could result in hyperthyroidism and hypothyroidism (Farebrother et al., Reference Farebrother, Zimmermann and Andersson2019; Leung and Braverman, Reference Leung and Braverman2014; Zimmermann, Reference Zimmermann2009). Subclinical hypothyroidism was also suggested to be attributed to excess intake of iodine via drinking groundwater with high iodide (I-) in China (Ma et al., Reference Ma, Yan, Han, Wang, Li, Zhou, Zheng, Hu, Borthwick and Zheng2022). Thus, both deficient and excess intakes of iodine have negative impacts on human health.
Radioactive isotopes of iodine also negatively impact human health. Iodine has a stable isotope 127I and a variety of radioactive isotopes. The latter was produced mainly by neutron-induced fission during the production of nuclear weapons and energy (Kaplan et al., Reference Kaplan, Denham, Zhang, Yeager, Xu, Sxhwehr, Li, Ho, Wellman and Santschi2014). Among the radioactive isotopes produced, 131I and 129I were the main radionuclides that could negatively affect human health. For example, a large quantity of 131I released from the explosion of the Chernobyl nuclear power plant caused thyroid cancer among the children who lived in the Chernobyl area when the incident occurred (Robbins and Schneider, Reference Robbins and Schneider1998).131I has a half-life of 8.02 days and high specific activity (4.59 × 103 TBqg-1). Thus, 131I was only a short-lived radioiodine (Hu and Moran, Reference Hu, Moran and Crabtree2010; Kaplan et al., Reference Kaplan, Denham, Zhang, Yeager, Xu, Sxhwehr, Li, Ho, Wellman and Santschi2014; Yeager et al., Reference Yeager, Amachi, Grandbois, Kaplan, Xu, Schwehr and Santschi2017). Another example is the 129I contamination in the Hanford Site at Washington State, USA, where subsurface 129I plumes were > 50 km2 and the 129I level in the groundwater was higher than the standard for 129I (<1pCi/L) listed in the US Federal Registry. The discharge of radioactive liquid during nuclear weapon production contributed to 129I contamination in the groundwater at the Hanford site. Currently, there is no existing method to remediate 129I levels below 1pCi/L in the groundwater (Zhang et al., Reference Zhang, Xu, Creeley, Ho, Li, Grandbois, Schwehr, Kaplan, Yeager and Wellman2013). Compared to 131I, 129I has a half-life of 1.57 × 107 years and low specific activity (6.6 MBqg-1) (Hu and Moran, Reference Hu, Moran and Crabtree2010; Kaplan et al., Reference Kaplan, Denham, Zhang, Yeager, Xu, Sxhwehr, Li, Ho, Wellman and Santschi2014; Yeager et al., Reference Yeager, Amachi, Grandbois, Kaplan, Xu, Schwehr and Santschi2017). Given its very long half-life, high toxicity to humans, highly specific accumulation in the human thyroid gland, high inventory in the Hanford Site, high mobility in groundwater and the uncertainty of its biogeochemical fate and transport in the environment, 129I is a primary risk driver at the Hanford Site (Kaplan et al., Reference Kaplan, Denham, Zhang, Yeager, Xu, Sxhwehr, Li, Ho, Wellman and Santschi2014).
The Earth’s oceans contain ~70% of the iodine on the Earth’s surface (Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Fuge and Johnson, Reference Fuge and Johnson2015). At the interface between surface air and surface water of oceans, ozone (O3) in the air interacts with I- in the oceans to produce molecular iodine (I2) and hypoiodous acid (HIO) (Carpenter et al., Reference Carpenter, MacDonald, Shaw, Kumar, Saunders, Parthipan, Wilson and Plane2013; Read et al., Reference Read, Mahajan, Carpenter, Evans, Faria, Heard, Hopkins, Lee, Moller and Lewis2008). The produced I2 and HIO in the oceans are then volatilized into the atmosphere. Up to 80% of atmospheric iodine is from volatilization of the I2 and HIO produced from the air-ocean interface (Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Carpenter et al., Reference Carpenter, MacDonald, Shaw, Kumar, Saunders, Parthipan, Wilson and Plane2013). This interfacial reaction between O3 and I- functions as a negative feedback mechanism for regulating atmospheric levels of O3 (Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Prados-Roman et al., Reference Prados-Roman, Cuevas, Fernandez, Kinnison, Lamarque and Saiz-Lopez2015). Furthermore, atmospheric iodine also contributes to ozone depletion (Fig. 1) (Koenig et al., Reference Koenig, Volkamer, Apel, Bresch, Cuevas, Dix, Eloranta, Fernandez, Hall and Hornbrook2021; Sherwen et al., Reference Sherwen, Evans, Carpenter, Schmidt and Mickley2017a; Sherwen et al., Reference Sherwen, Evans, Sommariva, Hollis, Ball, Monks, Reed, Carpenter, Lee and Forster2017b; Sherwen et al., Reference Sherwen, Schmidt, Evans, Carpenter, GroBmann, Eastham, Jacob, Dix, Koenig and Sinreich2016b; Yeager et al., Reference Yeager, Amachi, Grandbois, Kaplan, Xu, Schwehr and Santschi2017). Thus, atmospheric iodine impacts air quality and human health (Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Chance et al., Reference Chance, Baker, Carpenter and Jickells2014; Koenig et al., Reference Koenig, Volkamer, Apel, Bresch, Cuevas, Dix, Eloranta, Fernandez, Hall and Hornbrook2021). Given that it is the major source of aerosols (Fig. 1) (Gomez Martin et al., Reference Gomez Martin, Lewis, Blitz, Plane, Kumar, Francisco and Saiz-Lopez2020), atmospheric iodine may also have an impact on the climate (Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Chance et al., Reference Chance, Baker, Carpenter and Jickells2014; Yeager et al., Reference Yeager, Amachi, Grandbois, Kaplan, Xu, Schwehr and Santschi2017).
Bacterial roles in global biogeochemical cycling of iodine.
Bacteria play crucial and versatile roles in the global biogeochemical cycling of iodine (Amachi, Reference Amachi2008; Carpenter, Reference Carpenter2015; Luther III, Reference Luther2023; Yeager et al., Reference Yeager, Amachi, Grandbois, Kaplan, Xu, Schwehr and Santschi2017). The Gram-negative bacteria Denitromonas sp. IR-12, Pseudomonas sp. SCT and Shewanella oneidensis MR-1 can use small organic acids, such as acetate and lactate, to reduce iodate (IO3-) to I- directly via their IO3--reducing enzymes under anoxic conditions (Amachi et al., Reference Amachi, Kawaguchi, Muramatsu, Tsuchiya, Watanabe, Shinoyama and Fujii2007a; Guo et al., Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b; Reyes-Umana et al., Reference Reyes-Umana, Henning, Lee, Barnum and Coates2022; Shin et al., Reference Shin, Toporek, Mok, Maekawa, Lee, Howard and DiChristina2022; Yamazaki et al., Reference Yamazaki, Kashiwa, Horiuchi, Kasahara, Yamamura and Amachi2020). In addition to the direct reduction of IO3-, bacteria can also reduce IO3- indirectly via the reactive chemical species produced by the bacteria (Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c; Jiang et al., Reference Jiang, Qian, Cui, Jiang, Shi, Dong, Li and Wang2023d). For example, sulfate-reducing bacteria used lactate to reduce sulfate to sulfide biotically under anoxic conditions. The latter reduces IO3- to I- abiotically (Jiang et al., Reference Jiang, Qian, Cui, Jiang, Shi, Dong, Li and Wang2023d). Furthermore, bacteria can also oxidize I- to I2 under oxic conditions (Amachi, Reference Amachi2008; Luther III, Reference Luther2023). For example, IO3- was the predominant 129I species in the groundwater at the Hanford Site. Four bacterial isolates from the groundwater of the Hanford Site were able to oxidize I- to I2 (Lee et al., Reference Lee, Moser, Brooks, Saunders and Howard2020). Given that I2 could be oxidized to IO3- abiotically (Amachi, Reference Amachi2008), the I--oxidizing activity of these bacterial isolates might contribute to the IO3- accumulation in the groundwater at the Hanford Site (Lee et al., Reference Lee, Moser, Brooks, Saunders and Howard2020). Bacteria also accumulated and methylated I- (Amachi et al., Reference Amachi, Kamagata, Kanagawa and Muramatsu2001; Amachi et al., Reference Amachi, Mishima, Shinoyama, Muramatsu and Fujii2005b).
This review focuses on recent advances in the bacterial impacts on the global geochemical cycling of iodine, especially the molecular mechanisms by which bacteria mediate the biogeochemical transformation of iodine. These include recently discovered bacterial genes and enzymes directly involved in iodine biotransformation. Readers are encouraged to read other excellent reviews related to different aspects of biological contributions to the global cycling of iodine (Amachi, Reference Amachi2008; Carpenter, Reference Carpenter2015; Duborska et al., Reference Duborska, Balikova, Matulova, Zverina, Farkas, Littera and Urik2021; Duborska et al., Reference Duborska, Vojtkova, Matulova, Seda and Matus2023; Luther III, Reference Luther2023; Yeager et al., Reference Yeager, Amachi, Grandbois, Kaplan, Xu, Schwehr and Santschi2017).
The global geochemical cycle of iodine
Geochemical cycling of iodine occurs mainly in the oceans, which contain ~70% of the iodine on the Earth’s surface (Amachi, Reference Amachi2008; Carpenter, Reference Carpenter2015; Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Fuge and Johnson, Reference Fuge and Johnson2015; Luther III, Reference Luther2023; Yeager et al., Reference Yeager, Amachi, Grandbois, Kaplan, Xu, Schwehr and Santschi2017). Inorganic IO3- and I- are the two dominant species of iodine in the oceans, where their combined concentration is 0.45 −0.50 μmolL−1 (Chance et al., Reference Chance, Baker, Carpenter and Jickells2014). Organic iodine (org-I) also exists in the oceans. IO3-, I- and org-I concentrations in the oceans vary substantially (Amachi, Reference Amachi2008; Carpenter, Reference Carpenter2015; Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Yeager et al., Reference Yeager, Amachi, Grandbois, Kaplan, Xu, Schwehr and Santschi2017). In the surface layer of oceans, the concentrations of IO3- and I- are similar and higher than that of org-I. In the deep oceans, the concentrations decrease in the order of IO3- > I- > org-I (Fig. 1) (Carpenter, Reference Carpenter2015; Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Yeager et al., Reference Yeager, Amachi, Grandbois, Kaplan, Xu, Schwehr and Santschi2017). As mentioned previously, O3 oxidizes I- to I2 and HIO abiotically at the air-ocean interface. The produced I2 and HIO in the oceans are then volatilized into the air (Fig. 1) (Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Carpenter et al., Reference Carpenter, MacDonald, Shaw, Kumar, Saunders, Parthipan, Wilson and Plane2013; Prados-Roman et al., Reference Prados-Roman, Cuevas, Fernandez, Kinnison, Lamarque and Saiz-Lopez2015). HIO could be converted to IO3- and I- abiotically (Fig. 1) (Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021). Importantly, bacteria reduced IO3- to I- with HIO as a reaction intermediate under anoxic conditions (Guo et al., Reference Guo, Jiang, Peng, Zhong, Jiang, Jiang, Hu, Dong and Shi2022a; Guo et al., Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b; Reyes-Umana et al., Reference Reyes-Umana, Henning, Lee, Barnum and Coates2022; Yamazaki et al., Reference Yamazaki, Kashiwa, Horiuchi, Kasahara, Yamamura and Amachi2020) and oxidized I- to I2 in the oceans under oxic conditions, during which org-I is formed (Amachi et al., Reference Amachi, Muramatsu, Akiyama, Miyazaki, Yoshiki, Hanada, Kamagata, Ban-nai, Shinoyama and Fujii2005c). Microorganisms in the oceans also play key roles in org-I volatilization and can accumulate iodine (Fig. 1) (Amachi et al., Reference Amachi, Fujii, Shinoyama and Muramatsu2005a; Amachi et al., Reference Amachi, Kamagata, Kanagawa and Muramatsu2001; Amachi et al., Reference Amachi, Kasahara, Fujii, Shinoyama, Hanada, Kamagata, Ban-nai and Muramatsu2004; Amachi et al., Reference Amachi, Kimura, Muramatsu, Shinoyama and Fujii2007b; Amachi et al., Reference Amachi, Mishima, Shinoyama, Muramatsu and Fujii2005b).
Once volatilized into the air, I2, HIO and volatile org-I are photolyzed to atom iodine (I), which reacts with O3 to form iodine oxide radicals (IO). The latter reaction also results in O3 decay. IO further react with nitrogen and hydrogen oxides to form iodine-containing aerosols, which contribute to cloud formation (Fig. 1) (Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Prados-Roman et al., Reference Prados-Roman, Cuevas, Fernandez, Kinnison, Lamarque and Saiz-Lopez2015; Sherwen et al., Reference Sherwen, Evans, Carpenter, Schmidt and Mickley2017a; Sherwen et al., Reference Sherwen, Evans, Sommariva, Hollis, Ball, Monks, Reed, Carpenter, Lee and Forster2017b; Sherwen et al., Reference Sherwen, Evans, Spracklen, Carpenter, Chance, Baker, Schmidt and Bresch2016a; Sherwen et al., Reference Sherwen, Schmidt, Evans, Carpenter, GroBmann, Eastham, Jacob, Dix, Koenig and Sinreich2016b; Sipila et al., Reference Sipila, Sarnela, Jokinen, Henschel, Junninen, Kontkanen, Richyers, Kangasluoma, Franchin and Perakyla2016). The iodine-containing chemicals in the clouds cycle back to the oceans and land surface via dry and wet depositions (Fig. 1) (Carpenter et al., Reference Carpenter, Chance, Sherwen, Ball, Evans, Hepath, Hollis, Hughes and Jickells2021; Sherwen et al., Reference Sherwen, Evans, Spracklen, Carpenter, Chance, Baker, Schmidt and Bresch2016a). All of these reactions are abiotic. Thus, iodine in terrestrial environments originates mainly from oceans.
In addition to ocean-originated iodine, the human use of coal and fossil fuels also contributes to the inventory of terrestrial and atmospheric iodine (Fig. 1) (Fan et al., Reference Fan, Xu, Hou, Zhou, Zhang and Chen2023). Iodine is a biophilic element so becomes enriched in organic matter, which is the cause of iodine in coal and petroleum. Contact with shallow coal seams or the uplift from formation waters contributes to iodine enrichment in coal and crude oil (Chen et al., Reference Chen, Liu, Peng, Ning, Hou, Zhang and Xiao2016; Fehn et al., Reference Fehn, Tullai, Teng, Elmore and Kubik1987; Wu et al., Reference Wu, Deng, Zheng, Wang, Tang and Xiao2008; Wu et al., Reference Wu, Du, Deng, Wang, Xiao and Li2014). Org-I is the dominant species of iodine detected in terrestrial environments (Amachi et al., Reference Amachi, Kasahara, Hanada, Kamagata, Shinoyama, Fujii and Muramatsu2003; Biester et al., Reference Biester, Selimovic, Hemmerich and Petri2006; Fuge and Johnson, Reference Fuge and Johnson1986; Gilfedder et al., Reference Gilfedder, Petri and Biester2009; Keppler et al., Reference Keppler, Biester, Putschew, Silk, Scholer and Muller2004; Sheppard and Thibault, Reference Sheppard and Thibault1992; Shetaya et al., Reference Shetaya, Young, Watts, Ander and Bailey2012; Yamada et al., Reference Yamada, Kiriyama, Onagawa, Hisamori, Miyazaki and Yonebayashi1999). Similar to that in oceans, terrestrial bacteria also plays a crucial role in org-I formation; and some of the org-I is volatilized into the atmosphere (Amachi et al., Reference Amachi, Kasahara, Hanada, Kamagata, Shinoyama, Fujii and Muramatsu2003).
High concentrations of iodine in groundwater have been reported in Algeria, Argentina, Canada, Chile, China, Denmark and Japan, which is a major health concern to millions of people (Wang et al., Reference Wang, Li, Ma, Xie, Deng and Gan2021; Wang et al., Reference Wang, Zheng and Ma2018). The iodine in the groundwater originated from a variety of sources, such as Quaternary lacustrine sediments, ancient marine transgressions, salt water and soil deposition (Alvarez et al., Reference Alvarez, Reich, Perez-Fodich, Snyder, Muramatsu, Vargas and Fehn2015; Li et al., Reference Li, Wang, Xie, Zhang and Guo2013; Muramatsu et al., Reference Muramatsu, Fehn and Yoshida2001; Voutchkova et al., Reference Voutchkova, Kristiansen, Hansen, Ernstsen, Sorensen and Esbensen2014; Wang et al., Reference Wang, Li, Ma, Xie, Deng and Gan2021). The iodine was released to groundwater via burial dissolution and compaction-release (Wang et al., Reference Wang, Li, Ma, Xie, Deng and Gan2021). IO3-, I- and org-I all exist in groundwater and their concentrations vary considerably (Bagwell et al., Reference Bagwell, Zhong, Wells, Mitroshkov and Qafoku2019; Ma et al., Reference Ma, Yan, Han, Wang, Li, Zhou, Zheng, Hu, Borthwick and Zheng2022; Neeway et al., Reference Neeway, Kaplan, Bagwell, Rockhold, Szecsody, Truex and Qafoku2019; Wang et al., Reference Wang, Li, Ma, Xie, Deng and Gan2021; Zhang et al., Reference Zhang, Xu, Creeley, Ho, Li, Grandbois, Schwehr, Kaplan, Yeager and Wellman2013). For example, I- is the dominant species of iodine in the deep groundwater of the North China Plain, in which org-I is a minor species and no IO3- was detected (Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c). However, IO3- is the dominant species of iodine in groundwater at the Hanford site (Zhang et al., Reference Zhang, Xu, Creeley, Ho, Li, Grandbois, Schwehr, Kaplan, Yeager and Wellman2013). Bacteria are directly involved in IO3- reduction, I- oxidation and org-I formation in groundwater (Fig. 1) (Bagwell et al., Reference Bagwell, Zhong, Wells, Mitroshkov and Qafoku2019; Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c; Lee et al., Reference Lee, Moser, Brooks, Saunders and Howard2020).
Bacterial reduction of IO 3 -
Thermodynamically, IO3- is much more stable than I- in the environment (Luther III, Reference Luther2023). Bacterial reduction of IO3- contributes to the environmental formation of I-.
Direct reduction by IO3--respiring bacteria
Isolated from marine sediment, the Gram-negative bacterium Pseudomonas sp. SCT was the first microorganism experimentally demonstrated to be capable of respiring on IO3- for anaerobic growth in which acetate served as an electron donor (Yamazaki et al., Reference Yamazaki, Kashiwa, Horiuchi, Kasahara, Yamamura and Amachi2020):
$$ {\displaystyle \begin{array}{l}3{\mathrm{C}}_2{\mathrm{H}}_3{{\mathrm{O}}_2}^{-}+4{{\mathrm{I}\mathrm{O}}_3}^{-}+3{\mathrm{H}}^{+}\to 4{\mathrm{I}}^{-}+6{\mathrm{C}\mathrm{O}}_2\\ {}\hskip1em +\hskip2px 6{\mathrm{H}}_2\mathrm{O}\left({\Delta \mathrm{G}}^{0'}=-743\hskip0.3em \mathrm{kJ}/\mathrm{mol}\;\mathrm{acetate}\right)\end{array}} $$
Given that the reduced iodine species was not incorporated into any bacterial molecule, respiration of IO3- by Pseudomonas sp. SCT was also referred to as the dissimilatory reduction of IO3- (Fig. 2a) (Amachi et al., Reference Amachi, Kawaguchi, Muramatsu, Tsuchiya, Watanabe, Shinoyama and Fujii2007a; Yamazaki et al., Reference Yamazaki, Kashiwa, Horiuchi, Kasahara, Yamamura and Amachi2020). Subsequently, biochemical characterization identified a periplasmic iodate reductase (Idr) in Pseudomonas sp. SCT, which consisted of subunits of IdrA, IdrB, IdrP1 and IdrP2. The genes for these subunits, idrABP1P2, were clustered together. Phylogenetic analyses revealed that IdrAB belonged to the superfamily of dimethyl sulfoxide (DMSO) reductases that required molybdenum as a cofactor, while IdrP1P2 were the c-type cytochromes (c-Cyts) (Yamazaki et al., Reference Yamazaki, Kashiwa, Horiuchi, Kasahara, Yamamura and Amachi2020). Compared to that under the nitrate- or O2-respiring conditions, the mRNA levels of idrA, idrP1 and idrP2 were all elevated substantially under the IO3--respiring conditions (Yamazaki et al., Reference Yamazaki, Kashiwa, Horiuchi, Kasahara, Yamamura and Amachi2020). Further analyses detected H2O2 as a byproduct under the IO3--respiring conditions (Yamazaki et al., Reference Yamazaki, Kashiwa, Horiuchi, Kasahara, Yamamura and Amachi2020). Based on these results, Yamazaki et al. proposed that during IO3--respiration, Pseudomonas sp. SCT used IdrAB to reduce IO3- to HIO and H2O2, and IdrP1P2 to reduce H2O2 to H2O as a detoxification mechanism (Fig. 3a). The reduction intermediate HIO was proposed to be reduced to I-, probably by the Cld protein (Yamazaki et al., Reference Yamazaki, Kashiwa, Horiuchi, Kasahara, Yamamura and Amachi2020).
Bacteria-mediated direct and indirect reduction of IO3-: (a) IO3--respiring bacteria; (b) the Fe(III)-reducing bacterium Shewanella oneidensis MR-1, (c) the sulfate-reducing bacterium Desulfovibrio sp. B304, modified with permission from Jiang et al. (Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c) ©(2023) American Chemical Society.
The molecular mechanisms for the bacterial reduction of IO3-: (a) periplasmic reduction by IdrABP1P2, modified with permission from Reyes-Umana et al. (Reference Reyes-Umana, Henning, Lee, Barnum and Coates2022) ©(2022) Oxford University Press and (b) extracellular reduction by DmsEFAB and MtrCAB, modified with permission from Guo et al. (Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b) ©(2022) Blackwell Publishing LTD.
The idrABP1P2 gene cluster was also found in the genome of the IO3--respiring bacterium Denitromonas sp. IR-12 that was isolated from an estuarine sediment. The deletion of the idrA gene abolished the bacterial ability to reduce IO3-, which provided genetic evidence for the direct involvement of IdrA in IO3- reduction (Reyes-Umana et al., Reference Reyes-Umana, Henning, Lee, Barnum and Coates2022). Similar to that in Pseudomonas, sp. SCT, IdrAB of Denitromonas sp. IR-12 was proposed to reduce IO3- to HIO and H2O2. The latter was further detoxified to H2O by IdrP1P2. Given that no Cld homolog was identified in Denitromonas sp. IR-12, the HIO was proposed to be disproportionated abiotically into I- and IO3- at a ratio of 2:1 (Fig. 3a) (Reyes-Umana et al., Reference Reyes-Umana, Henning, Lee, Barnum and Coates2022). The idrABP1P2 gene cluster existed in phylogenetically diverse groups of bacterial genomes, which was probably attributed to the horizontal gene transfer of the idrABP1P2 gene cluster in different bacterial genomes (Reyes-Umana et al., Reference Reyes-Umana, Henning, Lee, Barnum and Coates2022; Sasamura et al., Reference Sasamura, Ohnuki, Kozai and Amachi2023). The bacteria with the idrABP1P2 gene cluster were predicted to be enriched in marine anoxic environments rich in nitrate and phosphate (Reyes-Umana et al., Reference Reyes-Umana, Henning, Lee, Barnum and Coates2022).
Comparative metagenomic analyses also identified the idrABP1P2 gene clusters in the groundwater of North China Plain, where iodine concentration was high; I- constituted up to 98% of iodine detected and IO3- was below the detectable level. Biochemical characterization of an identified idrABP1P2 gene cluster confirmed its IO3--reducing activity. Thus, the microorganisms with the idrABP1P2 gene clusters contributed at least in part to the I- formation in the groundwater of North China Plain (Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c).
Direct reduction by S. oneidensis MR-1
The dissimilatory Fe(III)- and DMSO-reducing bacterium S. oneidensis MR-1 respires on Fe(III)-containing minerals and DMSO extracellularly under anoxic conditions (Gralnick et al., Reference Gralnick, Vali, Lies and Newman2006; Myers and Nealson, Reference Myers and Nealson1988; Nealson et al., Reference Nealson, Belz and McKee2002). Crucial to the ability of S. oneidensis MR-1 to reduce Fe(III)-containing minerals and DMSO extracellularly are the MtrCAB and DmsEFAB protein complexes, respectively (Gralnick et al., Reference Gralnick, Vali, Lies and Newman2006; Shi et al., Reference Shi, Dong, Reguera, Beyenal, Lu, Liu, Yu and Fredrickson2016; White et al., Reference White, Edwards, Gomez-Perez, Richardson, Butt and Clarke2016). The MtrAB are the homologs of DmsEF and their function is to transfer electrons across the bacterial outer membrane. The extracellular MtrC is a terminal reductase of Fe(III)-containing minerals, while DmsAB is the extracellular terminal reductase of DMSO (Edwards et al., Reference Edwards, White, Butt, Richardson and Clarke2020; Gralnick et al., Reference Gralnick, Vali, Lies and Newman2006; Hartshorne et al., Reference Hartshorne, Reardon, Ross, Nuester, Clarke, Gates, Mills, Fredrickson, Zachara and Shi2009; White et al., Reference White, Shi, Shi, Wang, Dohnalkova, Marshall, Fredrickson, Zachara, Butt and Richardson2013; Xiong et al., Reference Xiong, Shi, Chen, Mayer, Lower, Londer, Bose, Hochella, Fredrickson and Squier2006). The mtrCAB and dmsEFAB genes are clustered together (Beliaev and Saffarini, Reference Beliaev and Saffarini1998; Gralnick et al., Reference Gralnick, Vali, Lies and Newman2006).
Under the anoxic condition, S. oneidensis MR-1 also reduced IO3- in a dissimilatory way with lactate as an electron donor. The deletion of the gene involved in nitrate reduction did not impact the ability of S. oneidensis MR-1 to reduce IO3- (Mok et al., Reference Mok, Toporek, Shin, Lee, Lee and DiChristina2018). However, deletions of the genes in the mtrCAB or dmsEFAB gene clusters all diminished the bacterial ability to reduce IO3- (Guo et al., Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b; Shin et al., Reference Shin, Toporek, Mok, Maekawa, Lee, Howard and DiChristina2022; Toporek et al., Reference Toporek, Mok, Shin, Lee, Lee and DiChristina2019). Further analyses showed that the dmsEFAB gene cluster was more dominant than the mtrCAB gene cluster in IO3- reduction. Neither HIO nor H2O2 were detected after the deletion of the dmsEFAB gene cluster, while HIO was still detectable, and H2O2 was accumulated after the deletion of the mtrCAB gene cluster (Guo et al., Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b). Protein purification and characterization revealed that the purified MtrC was a c-Cyt with intrinsic peroxidase activity (Shi et al., Reference Shi, Chen, Wang, Elias, Mayer, Gorby, Ni, Lower, Kennedy and Wunschel2006). Collectively, all these results showed that on the bacterial surface, DmsAB reduced IO3- to HIO and H2O2. MtrC then reduced H2O2 to H2O (Fig. 3b) (Guo et al., Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b). Similar to that produced with IdrABP1P2 (Fig. 3a) (Reyes-Umana et al., Reference Reyes-Umana, Henning, Lee, Barnum and Coates2022), the reduction intermediate HIO was probably disproportionated abiotically into I- and IO3- (Fig. 3b) (Guo et al., Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b). DmsEF and MtrAB transferred electrons from the periplasm and across the outer membrane to the DmsAB and MtrC, respectively (Fig. 3b) (Guo et al., Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b). The Mtr extracellular electron transfer pathway supplied electrons to DmsEFAB and MtrCAB for extracellular reduction of IO3- (Fig. 3b) (Guo et al., Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b; Shi et al., Reference Shi, Dong, Reguera, Beyenal, Lu, Liu, Yu and Fredrickson2016).
Many bacterial genomes contained both dmsEFAB and mtrCAB gene clusters, suggesting that they had the capability for extracellular reduction of IO3- (Guo et al., Reference Guo, Jiang, Peng, Zhong, Jiang, Jiang, Hu, Dong and Shi2022a). Indeed, other Shewanella species also reduced IO3- (Councell et al., Reference Councell, Landa and Lovley1997; Farrenkorf et al., Reference Farrenkorf, Dollopf, Chadhain, Luther and Nealson1997). These bacteria were found in a variety of ecosystems, such as oceans, lakes, rivers and subsurface rocks. Global distribution of the bacteria with the capability for extracellular reduction of IO3-, especially their widespread occurrence in oceans, suggested the importance of these bacteria in the global geochemical cycling of iodine (Guo et al., Reference Guo, Jiang, Peng, Zhong, Jiang, Jiang, Hu, Dong and Shi2022a).
Notably, DmsAB of S. oneidensis MR-1 and IdrAB of Pseudomonas sp. SCT and Denitromonas sp. IR-12 are members of the DMSO reductase superfamily, whose diverse functions range from sulfur and nitrate reductions to sulfite and arsenite oxidations. How the DmsAB and IdrAB reduce IO3- is currently unknown (Wells et al., Reference Wells, Kim, Akob, Basu and Stolz2023). Furthermore, DmsEF and Mtr CAB of S. oneidensis MR-1 share no sequence similarity to IdrP1P2 of Pseudomonas sp. SCT and Denitromonas sp. IR-12. Thus, IO3- reduction by IdrABP1P2 and DmsEFAB/MtrCAB are the results of convergent evolution. Moreover, DmsEFAB and MtrCAB of S. oneidensis MR-1 functioned primarily for the extracellular respiration of DMSO and Fe(III)-containing minerals, respectively (Gralnick et al., Reference Gralnick, Vali, Lies and Newman2006; Shi et al., Reference Shi, Dong, Reguera, Beyenal, Lu, Liu, Yu and Fredrickson2016; White et al., Reference White, Edwards, Gomez-Perez, Richardson, Butt and Clarke2016). No cell growth was observed for S. oneidensis MR-1 during dissimilatory reduction of IO3- (Guo et al., Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b; Toporek et al., Reference Toporek, Mok, Shin, Lee, Lee and DiChristina2019). Thus, the extracellular reduction of IO3- by S. oneidensis MR-1 was considered a fortuitous reaction (Guo et al., Reference Guo, Jiang, Hu, Jiang, Dong and Shi2022b). Nevertheless, this fortuitous reaction may help bacterial survival in environments where IO3- is available but DMSO and Fe(III) are absent.
Indirect reduction by S. oneidensis MR-1 in the presence of Fe(III)-containing minerals
In soils, sediments and subsurfaces rich in Fe(III)-containing minerals, IO3- and org-I adsorb to the surface of minerals (Dai et al., Reference Dai, Zhang and Zhu2004; Fuge and Johnson, Reference Fuge and Johnson1986; Guido-Garcia et al., Reference Guido-Garcia, Law, Lloyd, Lythgoe and Morris2015; Li et al., Reference Li, Jiang, Xie and Wang2022; Li et al., Reference Li, Wang, Xue, Xie, Siebecker, Sparks and Wang2020; Shetaya et al., Reference Shetaya, Young, Watts, Ander and Bailey2012; Wang et al., Reference Wang, Li, Ma, Xie, Deng and Gan2021). Reductive dissolution of Fe(III)-minerals by the Fe(III)-reducing microorganisms results in the release of IO3- and org-I from the mineral surface to the solution (Guido-Garcia et al., Reference Guido-Garcia, Law, Lloyd, Lythgoe and Morris2015; Jiang et al., Reference Jiang, Cui, Qian, Jiang, Shi, Dong, Li and Wang2023b; Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c; Li et al., Reference Li, Jiang, Xie and Wang2022; Li et al., Reference Li, Wang, Xue, Xie, Siebecker, Sparks and Wang2020). Furthermore, Fe(II), the product of Fe(III) reduction, also reduces IO3- abiotically (Councell et al., Reference Councell, Landa and Lovley1997). The high concentration of iodine in the groundwater of North China Plain was believed to have originated from the iodine adsorbed on Fe(III)-containing minerals (Li et al., Reference Li, Jiang, Xie and Wang2022; Xue et al., Reference Xue, Xie, Li, Wang and Wang2022). Comparative metagenomic analyses of groundwater with a high concentration of I- from the North China Plain identified MtrCAB and OmcS homologs (Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c). Similar to MtrCAB of S. oneidensis MR-1, OmcS of the dissimilatory Fe(III)-reducing bacterium Geobacter sulfurreducens was directly involved in the extracellular reduction of Fe(III)-containing minerals (Jiang et al., Reference Jiang, He, Luo, Peng, Jiang, Hu, Qi, Dong, Dong and Shi2023a; Mehta et al., Reference Mehta, Coppi, Childers and Lovley2005). Thus, Fe(III)-reducing bacteria may also contribute to the formation of high I--containing groundwater in the North China Plain (Fig. 2b) (Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c).
Further investigation showed that Fe(II) abiotically reduced IO3- to HIO and I- at a ratio of 1:2. The produced HIO was then disproportionated into I- and IO3- at a ratio of 2:1 (Jiang et al., Reference Jiang, Cui, Qian, Jiang, Shi, Dong, Li and Wang2023b). IO3 reductions in the presence of water-soluble Fe(III)-citrate or different forms of Fe(III)-containing minerals by S. oneidensis MR-1, its mutants without dmsEFAB or mtrCAB and Shewanella sp. ANA-3, which contained only a mtrCAB homolog, was also comparatively analysed. The results consistently demonstrated that IO3- was abiotically reduced by the Fe(II) produced from bacteria-mediated Fe(III) reduction. The indirect reduction of IO3- by S. oneidensis MR-1 via biogenic Fe(II) was more predominant than the direct reduction of IO3- by S. oneidensis MR-1 under the conditions rich in Fe(III). Direct reduction of IO3- by S. oneidensis MR-1 via DmsEFAB and MtrCAB occurred mainly when the Fe(III) level was low. Compared to that with Fe(III)-citrate, the Fe(II) produced with Fe(III)-containing minerals reduced IO3- more efficiently. Collectively, these results demonstrated that Fe(III)-reducing bacteria, such as S. oneidensis MR-1, Shewanella sp. ANA-3 and probably G. sulfurreducens reduced IO3- indirectly via the Fe(II) from Fe(III) reduction (Fig. 2b) (Jiang et al., Reference Jiang, Cui, Qian, Jiang, Shi, Dong, Li and Wang2023b).
Direct and indirect reduction by sulfate-reducing bacteria
The dissimilatory sulfate-reducing bacterium Desulfovibrio desulfuricans was among the first microorganisms experimentally demonstrated to be capable of reducing IO3- to I- directly under anoxic conditions (Councell et al., Reference Councell, Landa and Lovley1997). Similar to Fe(II), the sulfide, which was a byproduct of sulfate reduction, abiotically reduced IO3- to I- (Councell et al., Reference Councell, Landa and Lovley1997). Sulfur isotope and chemical analyses reveal that the δ34SSO4 value of groundwater was positively correlated with the concentrations of iodine, I- and sulfide in the aquifer of the North China Plain (Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c; Jiang et al., Reference Jiang, Qian, Cui, Jiang, Shi, Dong, Li and Wang2023d). Metagenomic and qPCR analyses also revealed that the concentrations of iodine and I- in these groundwaters were positively correlated with the abundance of microbial genes directly involved in sulfate reduction, such as dsrA and dsrB, and sulfate-reducing bacteria (Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c; Jiang et al., Reference Jiang, Qian, Cui, Jiang, Shi, Dong, Li and Wang2023d). Further analyses showed that the dissimilatory sulfate-reducing bacterium Desulfovibrio sp. B304, which was isolated from the groundwater of high iodine in Northern China, reduced IO3- to I- in the absence of sulfate. The addition of molybdenum also improved the IO3- reduction by Desulfovibrio sp. B304, suggesting that the direct reduction of IO3- by Desulfovibrio sp. B304 was probably mediated by the molybdenum-dependent DMSO reductase. In the presence of sulfate, the rate and extent of reducing IO3- by Desulfovibrio sp. B304 increased substantially. This enhanced reduction was attributed to the abiotic reduction of IO3- by the sulfide produced from the sulfate reduction (Jiang et al., Reference Jiang, Qian, Cui, Jiang, Shi, Dong, Li and Wang2023d). Thus, sulfate-reducing bacteria reduced IO3- directly, probably via their molybdenum-dependent DMSO reductases, as well as indirectly via the sulfide from sulfate reduction, which all contributed to the I- enrichment in the groundwater of the North China Plain and probably other sites rich in I- (Fig. 2c) (Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c; Jiang et al., Reference Jiang, Qian, Cui, Jiang, Shi, Dong, Li and Wang2023d).
In addition to IO3- reduction, sulfate-reducing bacteria might also mediate org-I dehalogenation directly via their dehalogenases and the reductive dissolution of the Fe(III)-containing minerals adsorbed with iodine indirectly via sulfide from sulfate reduction in the groundwater of high I- from the North China Plain, which could contribute to the I- enrichment in the groundwater (Jiang et al., Reference Jiang, Huang, Jiang, Dong, Shi, Li and Wang2023c; Jiang et al., Reference Jiang, Qian, Cui, Jiang, Shi, Dong, Li and Wang2023d).
Bacterial oxidation of I -
The first I--oxidizing bacterium was isolated from a marine aquarium where fish death was associated with the elevated I2 level in the aquarium water (Gozlan, Reference Gozlan1968; Gozlan and Margalith, Reference Gozlan and Margalith1973;, Reference Gozlan and Margalith1974). Subsequently, I--oxidizing bacteria were isolated from the brine waters and biofilms of natural gas plants, seawaters, marine sediments, soils, groundwater from the Hanford Site and subsurface sediments of contaminated 129I in the Savanna River Site, South Carolina, USA (Amachi et al., Reference Amachi, Fujii, Shinoyama and Muramatsu2005a; Amachi et al., Reference Amachi, Kasahara, Hanada, Kamagata, Shinoyama, Fujii and Muramatsu2003; Amachi et al., Reference Amachi, Muramatsu, Akiyama, Miyazaki, Yoshiki, Hanada, Kamagata, Ban-nai, Shinoyama and Fujii2005c; Arakawa et al., Reference Arakawa, Akiyama, Furukawa, Suda and Amachi2012; Fuse et al., Reference Fuse, Inoue, Murakami, Takimura and Yamaoka2003; Hughes et al., Reference Hughes, Barton, Hepach, Chance, Pickering, Hogg, Pommerening-Roser, Wadley, Stevens and Jickells2021; Iino et al., Reference Iino, Ohkuma, Kamagata and Amachi2016; Lee et al., Reference Lee, Moser, Brooks, Saunders and Howard2020; Li et al., Reference Li, Brinkmeyer, Jones, Zhang, Xu, Ho, Schwehr, Kaplan, Santschi, Yeager, Kawaguchi, Sato, Yokokawa, Itai, Nguyen, Ono and Tanabe2012a; Zhao et al., Reference Zhao, Lim, Miyanaga and Tanji2013).
Direct oxidation by bacterial multicopper oxidases
The I--oxidizing bacteria strain Iodidimonas sp. Q-1 and Roseovarius sp. strain A-2 oxidized I- extracellularly to I2 via their multicopper iodide oxidases with O2 as the electron acceptor (Fig. 4a) (Amachi and Iino, Reference Amachi and Iino2022; Amachi et al., Reference Amachi, Muramatsu, Akiyama, Miyazaki, Yoshiki, Hanada, Kamagata, Ban-nai, Shinoyama and Fujii2005c; Shiroyama et al., Reference Shiroyama, Kawasaki, Unno and Amachi2015; Suzuki et al., Reference Suzuki, Eda, Ohsawa, Kanesaki, Yoshikawa, Tanaka, Muramatsu, Yoshikawa, Sato and Fujii2012). Once I2 was formed, following its hydrolysis to HIO and I-, the disproportionation reaction of HIO to form IO3- and I- might spontaneously occur (Amachi and Iino, Reference Amachi and Iino2022). The proposed sum of this reaction is:
$$ 4{\mathrm{I}}^{\hbox{-} }+{\mathrm{O}}_2+4{\mathrm{H}}^{+}\to 2{\mathrm{I}}_2+2{\mathrm{H}}_2\mathrm{O}\;\left({\Delta \mathrm{G}}^{0'}=-101.57\hskip0.5em \mathrm{kJ}/\mathrm{mol}\;{\mathrm{I}}^{\hbox{-}}\right) $$
Bacterial oxidation of I-: (a) extracellular multicopper iodide oxidase; (b) ammonia-oxidizing bacteria; (c) extracellular reactive oxygen species. Abbreviations: Amo: ammonia monooxygenase; HP, heme peroxidase; Iox: iodide oxidase; NOX, NADPH oxidase.
The multicopper iodide oxidases of these bacteria consisted of at least two subunits–IoxA and IoxC, whose genes were clustered together with other genes, such as ioxB and ioxDEF (Shiroyama et al., Reference Shiroyama, Kawasaki, Unno and Amachi2015; Suzuki et al., Reference Suzuki, Eda, Ohsawa, Kanesaki, Yoshikawa, Tanaka, Muramatsu, Yoshikawa, Sato and Fujii2012). IoxA and IoxC homologs were found in other I--oxidizing bacteria, and multicopper iodide oxidase activity was also detected in the I--oxidizing bacteria isolated from the Hanford Site (Lee et al., Reference Lee, Moser, Brooks, Saunders and Howard2020; Shiroyama et al., Reference Shiroyama, Kawasaki, Unno and Amachi2015; Suzuki et al., Reference Suzuki, Eda, Ohsawa, Kanesaki, Yoshikawa, Tanaka, Muramatsu, Yoshikawa, Sato and Fujii2012). In addition to I2, volatile org-I compounds such as diiodomethane (CH2I2) and chloroiodomethane (CH2ClI) were also produced by I--oxidizing bacteria during I- oxidation (Amachi et al., Reference Amachi, Fujii, Shinoyama and Muramatsu2005a; Amachi et al., Reference Amachi, Kasahara, Hanada, Kamagata, Shinoyama, Fujii and Muramatsu2003; Amachi et al., Reference Amachi, Muramatsu, Akiyama, Miyazaki, Yoshiki, Hanada, Kamagata, Ban-nai, Shinoyama and Fujii2005c; Fuse et al., Reference Fuse, Inoue, Murakami, Takimura and Yamaoka2003). Notably, microbial multicopper iodide oxidase activity was detected in soils. The addition of bacterial multicopper oxidase to the soil samples with I- and organic matter oxidized I- to I2 and HIO that were eventually incorporated into the organic matter of soil to form org-I, some of which are immobilized (Seki et al., Reference Seki, Oikawa, Taguchi, Ohnuki, Muramatsu, Sakamoto and Amachi2013; Xu et al., Reference Xu, Miller, Zhang, Li, Ho, Schwehr, Kaplan, Otosaka, Roberts and Brinkmeyer2011a; Xu et al., Reference Xu, Zhang, Ho, Miller, Roberts, Li, Schwehr, Otosaka, Kaplan and Brinkmeyer2011b; Zhang et al., Reference Zhang, Xu, Creeley, Ho, Li, Grandbois, Schwehr, Kaplan, Yeager and Wellman2013).
As a bactericide, iodine kills bacteria. Although the exact killing mechanism remains uncertain, I2, HIO and probably I3- have all been proposed to contribute to bacterial killing (Gottardi, Reference Gottardi1999; Hickey et al., Reference Hickey, Panicucci, Duan, Dinehart, Murphy, Kessler and Gottardi1997). Compared to non-I--oxidizing bacteria, I--oxidizing bacteria were more tolerant to I2 (Arakawa et al., Reference Arakawa, Akiyama, Furukawa, Suda and Amachi2012; Zhao et al., Reference Zhao, Lim, Miyanaga and Tanji2013). The I--oxidizing bacteria with multicopper oxidases killed other non- I--oxidizing bacteria in the presence of I-, probably via the I2 produced from I- oxidation (Yuliana et al., Reference Yuliana, Ebihara, Suzuki, Shimonaka and Amachi2015; Zhao et al., Reference Zhao, Lim, Miyanaga and Tanji2013). This antibacterial capability might improve the ability of I--oxidizing bacteria to compete with other bacteria in the presence of I- (Yuliana et al., Reference Yuliana, Ebihara, Suzuki, Shimonaka and Amachi2015).
Direct oxidation by ammonia-oxidizing bacteria
Global modeling of iodine has suggested that I- oxidation to IO3- was probably linked to bacterial nitrification in oceans (Truesdale et al., Reference Truesdale, Watts and Rendell2001; Wadley et al., Reference Wadley, Stevens, Jickells, Hughes, Chance, Hepath, Tinel and Carpenter2020). Bacterial nitrification is mediated by two different groups of bacteria: ammonia-oxidizing bacteria and nitrite-oxidizing bacteria. The former oxidizes ammonia to nitrite, while the latter oxidizes nitrite to nitrate (Kowalchuk and Stephen, Reference Kowalchuk and Stephen2001). Indeed, the marine ammonia-oxidizing bacteria Nitrosomonas sp. (Nm51) and Nitrosoccocus oceani (Nc10) oxidizes I- to IO3- (Fig. 4b). However, no I- oxidation activity has been detected in the nitrite-oxidizing bacteria Nitrospira marina, Nitrospina gracilis or Nitrococcus mobilis. Hence it was proposed that Nitrosomonas sp. (Nm51) and Nitrosoccocus oceani (Nc10) used ammonia-oxidizing enzymes to oxidize I- (Hughes et al., Reference Hughes, Barton, Hepach, Chance, Pickering, Hogg, Pommerening-Roser, Wadley, Stevens and Jickells2021). The proposed electron acceptor for this reaction is O2:
$$ 2{\mathrm{I}}^{\hbox{-} }+3{\mathrm{O}}_2\to 2{{\mathrm{I}\mathrm{O}}_3}^{\hbox{-}}\left({\Delta \mathrm{G}}^{0'}=-100.88\hskip0.4em \mathrm{kJ}/\mathrm{mol}\;{\mathrm{I}}^{\hbox{-}}\right) $$
Moreover, a low iodide level has been found in the ocean depths where the nitrite level is high, which is consistent with the I- oxidation driven by ammonia-oxidizing bacteria in the oceans (Moriyasu et al., Reference Moriyasu, Bolster, Hardisty, Kadko, Stephens and Moffett2023).
Indirect oxidation by the extracellular reactive species produced by bacteria
Many bacteria produce extracellular reactive oxygen species, such as superoxide and H2O2, under oxic conditions (Bond et al., Reference Bond, Hansel and Voelker2020; Diaz et al., Reference Diaz, Hansel, Voelker, Mendes, Andeer and Zhang2013; Hansel and Diaz, Reference Hansel and Diaz2021). In the presence of H2O2, the bacterial isolates from the Savanna River Site oxidized I- to triiodide (I3-). This H2O2-dependent oxidation of I- was facilitated by the organic acids produced by bacterial isolates. The organic acids produced lowered the pH of the reaction solution and reacted with H2O2 to form peroxycarboxylic acids that were stronger oxidants than H2O2, which all contributed to I- oxidation to I3- (Fig. 4c) (Li et al., Reference Li, Yeager, Brinkmeyer, Zhang, Ho, Xu, Jones, Schwehr, Otosaka and Roberts2012b). Similarly, the marine bacterium Roseobacter sp. AzwK-3b produced extracellular superoxide that oxidized I- (Li et al., Reference Li, Daniel, Creeley, Grandbois, Zhang, Xu, Ho, Schwehr, Kaplan and Santschi2014).
Bacterial accumulation of I -
As a biophilic element, iodine accumulates in the cells of different organisms (Amachi, Reference Amachi2008). For example, humans and other mammals accumulate iodine in the thyroid gland. Accumulation occurs in the thyroid follicular cells that use the Na+ and I- co-transporter located at the basolateral membrane to transport I- into the cells. Once inside thyroid follicular cells, I- is oxidized to I2 by the thyroid peroxidase in the presence of H2O2. The I2 is finally incorporated into thyroid hormones T3 and T4 (Smyth and Dwyer, Reference Smyth and Dwyer2002). Brown algae also accumulate a significant amount of iodine, and the iodine content of brown algae Laminaria digitata could be as great as 5% of its dry weight (Gall et al., Reference Gall, Kupper and Kloareg2004). In the presence of H2O2, the extracellular vanadium iodoperoxidase of L. digitata oxidized I- to I2, HIO and I3- that were then transported into algal cells (Kupper and Carrano, Reference Kupper and Carrano2019; Kupper et al., Reference Kupper, Schweigert, Gall, Legendre, Vilter and Kloareg1998; Verhaeghe et al., Reference Verhaeghe, Fraysse, Guerquin-Kern, Wu, Deves, Mioskowski, Leblanc, Ortega, Ambroise and Potin2008). Inside the cells of L. digitata, I- was the major species of iodine, while org-I was the minor species (Gall et al., Reference Gall, Kupper and Kloareg2004). Brown algae accumulated I- as a defense mechanism against infection of microbial pathogens, as well as an antioxidant in response to oxidative stress (Kupper and Carrano, Reference Kupper and Carrano2019).
Arenibacter sp. strain C-21, which was isolated from the surface of marine sediments, was the first I--accumulating bacterium reported (Amachi et al., Reference Amachi, Mishima, Shinoyama, Muramatsu and Fujii2005b; Ito et al., Reference Ito, Nakajima, Yamamura, Tomita, Suzuki and Amachi2016). The uptake of I- by Arenibacter sp. strain C-21 is dependent on glucose, O2 and H2O2 (Amachi et al., Reference Amachi, Kimura, Muramatsu, Shinoyama and Fujii2007b; Amachi et al., Reference Amachi, Mishima, Shinoyama, Muramatsu and Fujii2005b). It was proposed that the oxidation of glucose by Arenibacter sp. strain C-21 produced extracellular H2O2. The extracellular vanadium iodoperoxidase of Arenibacter sp. strain C-21 used H2O2 to oxidize I- to HIO, which was then transported into bacterial cells (Amachi et al., Reference Amachi, Kimura, Muramatsu, Shinoyama and Fujii2007b). Indeed, the genome of Arenibacter sp. strain C-21 contains at least five putative genes for vanadium-dependent iodoperoxidase (Ito et al., Reference Ito, Nakajima, Yamamura, Tomita, Suzuki and Amachi2016). The I- -accumulating bacteria have also been isolated from subsurface sediments of the Savanna River Site and the Lastensuo Bog, Finland (Li et al., Reference Li, Brinkmeyer, Jones, Zhang, Xu, Schwehr, Santschi, Kaplan and Yeager2011; Lusa et al., Reference Lusa, Lehto, Aromaa, Knuutinen and Bomberg2016). Some cyanobacteria, such as Nostoc commune, Scytonema javanicum and Stigonema ocellatum, display a high ability to accumulate I- (Fukuda et al., Reference Fukuda, Iwamoto, Atsumi, Yokoyama, Nakayama, Ishida, Inouye and Shiraiwa2014).
Bacterial formation of org-I
A variety of terrestrial and aquatic bacteria produce volatile org-I (Amachi et al., Reference Amachi, Kamagata, Kanagawa and Muramatsu2001; Amachi et al., Reference Amachi, Kasahara, Fujii, Shinoyama, Hanada, Kamagata, Ban-nai and Muramatsu2004; Brownell et al., Reference Brownell, Moore and Cullen2010; Fujimori et al., Reference Fujimori, Yokoyama, Kurihara, Tamegai and Hashimoto2012; Fuse et al., Reference Fuse, Inoue, Murakami, Takimura and Yamaoka2003; Gomez-Consarnau et al., Reference Gomez-Consarnau, Klein, Cutter and Sanudo-Wilhelmy2021; Hirata et al., Reference Hirata, Ikeda, Fukuda, Abe, Sawada and Hashimoto2017; Smythe-Wright et al., Reference Smythe-Wright, Boswell, Breithaupt, Davidson, Dimmer and Diaz2006). As mentioned above, the I--oxidizing bacteria also produce org-I during I- oxidation in addition to I2 (Amachi et al., Reference Amachi, Fujii, Shinoyama and Muramatsu2005a; Amachi et al., Reference Amachi, Kasahara, Hanada, Kamagata, Shinoyama, Fujii and Muramatsu2003; Amachi et al., Reference Amachi, Muramatsu, Akiyama, Miyazaki, Yoshiki, Hanada, Kamagata, Ban-nai, Shinoyama and Fujii2005c; Fuse et al., Reference Fuse, Inoue, Murakami, Takimura and Yamaoka2003). Once accumulated inside bacterial cells, some of the HIO was believed to be transformed into org-I (Amachi et al., Reference Amachi, Kimura, Muramatsu, Shinoyama and Fujii2007b). Thus, HIO and I2 produced during IO3- reduction and I- oxidation contributed to org-I formation (Luther III, Reference Luther2023)
In the Arabidopsis plant, the deletion of a gene for methyltransferase increased the iodine content in the plant cells, demonstrating the crucial role of methyltransferase in iodine metabolism in plant cells (Landini et al., Reference Landini, Gonzali, Kiferle, Tonacchera, Agretti, Dimida, Vitti, Alpi, Pinchera and Perata2012). Methyltransferases were proposed to use S-adenosyl-L-methionine as a methyl donor for methylating I- (Duborska et al., Reference Duborska, Balikova, Matulova, Zverina, Farkas, Littera and Urik2021; Itoh et al., Reference Itoh, Toda, Matsuda, Negishi, Taniguchi and Ohsawa2009). Indeed, the cell extracts of the I--methylating bacterium Rhizobium sp. strain MRCD 19 possesses the enzymatic activity that catalyzes I- methylation in the presence of S-adenosyl-L-methionine, which suggests a similar role of bacterial methyltransferases in I- methylation (Amachi et al., Reference Amachi, Kamagata, Kanagawa and Muramatsu2001). In the presence of H2O2, the vanadium-dependent iodoperoxidases were also involved in methylating I- by brown algae L. digitata (Colin et al., Reference Colin, Leblanc, Wagner, Delage, Leize-Wagner, Van Dorsselaer, Kloareg and Potin2003). The molecular mechanisms underlying bacterial formation of org-I are, however, currently unknown.
Perspectives
Bacteria play crucial and versatile roles in the global geochemical cycling of iodine via IO3- reduction, I- oxidation and accumulation as well as org-I formation. Recently, substantial advances have been made in the understanding of the molecular mechanisms used by bacteria for reducing IO3-, as well as the importance of ammonia-oxidizing bacteria in I- oxidation, which provide new insights into the bacterial roles in the global geochemical cycling of iodine.
Despite these progresses, key knowledge gaps still remain regarding bacterial roles in the biogeochemical cycling of iodine. For example, the ecological importance of IO3--reducing, Fe(III)-reducing or sulfate-reducing bacteria in the biogeochemical cycling of iodine is currently unknown. Whether the I--oxidizing bacteria can conserve energy for chemolithoautotrophic growth remains to be demonstrated. Additionally, further investigation should also focus on whether bacterial iodine-transforming activity is fortuitous, mixotrophic or syntrophic.
Bridging these knowledge gaps will not only shed new light on bacterial roles in the global geochemical cycling of iodine but also help develop the models for predicting the biogeochemical fate and transport of 129I in the contaminated sites and iodine cycling in oceans.
Acknowledgments
This work was supported by the National Natural Science Foundation of China (42272353, 42277065) and the Fundamental Research Funds for the Universities of Chinese Central Government, China University of Geosciences-Wuhan (122-G1323533057).
Competing interests
The authors declare none.
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