The Crucial and Versatile Roles of Bacteria in Global Biogeochemical Cycling of Iodine

Iodine (I) is a trace element of significant importance to human health and the environment. It is a major component of human thyroid hormones, such as thyroxine (T4) and triiodothyronine (T3), directly influencing thyroid function. However, approximately 1.9 billion people worldwide are affected by Iodine Deficiency Disorder (IDD), with symptoms including goiter and cretinism. While IDD can be effectively prevented through salt iodization and food fortification, excessive iodine intake can lead to hyperthyroidism or hypothyroidism. Additionally, radioactive iodine isotopes (such as 131I and 129I) pose serious threats to human health, particularly when released during nuclear accidents or weapons production, potentially causing thyroid cancer and other diseases.

In nature, iodine primarily exists in the forms of iodate (IO3-), iodide (I-), and organic iodine (Org-I). The oceans are the main reservoir of iodine on Earth, with approximately 70% of the planet’s surface iodine stored in marine environments. Bacteria play a crucial role in the biogeochemical cycling of iodine, including the reduction of iodate, oxidation and accumulation of iodide, and formation of organic iodine. However, the specific molecular mechanisms by which bacteria mediate these processes and their ecological significance in the global iodine cycle remain largely unknown. Therefore, this article aims to review the key roles of bacteria in the biogeochemical cycling of iodine, particularly focusing on recent advances in understanding the molecular mechanisms of bacterial-mediated iodine transformations.

Source of the Paper

This paper was co-authored by Zhou Jiang, Yongguang Jiang, Yidan Hu, Yiran Dong, and Liang Shi, who are affiliated with the School of Environmental Studies, China University of Geosciences (Wuhan), the State Key Laboratory of Biogeology and Environmental Geology, the Key Laboratory of Source Apportionment and Control of Aquatic Pollution of the Ministry of Ecology and Environment, and the Hubei Key Laboratory of Yangtze Catchment Environmental Aquatic Science. The paper was published on August 30, 2024, in the journal Geo-Bio Interfaces, titled “The Crucial and Versatile Roles of Bacteria in Global Biogeochemical Cycling of Iodine.”

Main Content of the Paper

1. The Role of Bacteria in Iodate Reduction

Iodate (IO3-) is more stable than iodide (I-) in the environment, and bacteria contribute to the formation of iodide through the reduction of iodate. This process occurs through two main pathways: direct reduction and indirect reduction.

Direct Reduction: Certain bacteria, such as Pseudomonas sp. SCT and Denitromonas sp. IR-12, reduce iodate to iodide under anoxic conditions using iodate reductases (e.g., IdrABP1P2). IdrAB belongs to the dimethyl sulfoxide (DMSO) reductase superfamily and requires molybdenum as a cofactor, while IdrP1P2 are c-type cytochromes (c-Cyts). During reduction, iodate is first reduced to hypoiodous acid (HIO) and hydrogen peroxide (H2O2), after which H2O2 is reduced to water, and HIO is disproportionated into iodide and iodate through abiotic reactions.

Indirect Reduction: Iron-reducing bacteria (e.g., Shewanella oneidensis MR-1) and sulfate-reducing bacteria (e.g., Desulfovibrio sp. B304) indirectly reduce iodate through their reduction products, Fe(II) and sulfide. Fe(II) and sulfide abiotically reduce iodate to iodide. This process is particularly important in environments rich in iron and sulfate, especially in groundwater.

2. The Role of Bacteria in Iodide Oxidation

Under oxic conditions, bacteria oxidize iodide to molecular iodine (I2) using multicopper iodide oxidases (e.g., IoxAC). Additionally, ammonia-oxidizing bacteria (e.g., Nitrosomonas sp. NM51 and Nitrosococcus oceani NC10) oxidize iodide to iodate using their ammonia-oxidizing enzymes. Reactive oxygen species (e.g., superoxide and H2O2) produced by bacteria can also oxidize iodide to triiodide (I3-) under abiotic conditions.

3. The Role of Bacteria in Iodide Accumulation

Certain bacteria (e.g., Arenibacter sp. Strain C-21) oxidize iodide to hypoiodous acid (HIO) using extracellular vanadium iodoperoxidases and subsequently transport HIO into cells for accumulation. This process is analogous to iodide accumulation in human thyroid cells and may serve as a defense mechanism against microbial pathogens.

4. The Role of Bacteria in Organic Iodine Formation

Bacteria methylate iodide to form organic iodine (e.g., CH3I) using methyltransferases. Additionally, bacteria produce various organic iodine compounds during iodide oxidation. These organic iodine compounds are widely present in marine and terrestrial environments and play a significant role in the global iodine cycle.

Significance and Value of the Paper

This paper systematically reviews the key roles of bacteria in the biogeochemical cycling of iodine, particularly focusing on recent advances in understanding the molecular mechanisms of bacterial-mediated iodine transformations. By elucidating the specific mechanisms by which bacteria reduce iodate, oxidize and accumulate iodide, and form organic iodine, this paper provides new insights into the global iodine cycle. Furthermore, it highlights critical knowledge gaps in current research, such as the ecological importance of iodate-reducing, iron-reducing, and sulfate-reducing bacteria in the iodine cycle, as well as whether iodide-oxidizing bacteria can conserve energy for chemolithoautotrophic growth. Future research should further explore these questions to enhance our understanding of the global iodine cycle and develop models for predicting the biogeochemical fate and transport of 129I in contaminated sites.

Research Highlights

  1. Elucidation of Molecular Mechanisms: This paper details the molecular mechanisms by which bacteria reduce iodate, oxidize and accumulate iodide, and form organic iodine, particularly focusing on the roles of IdrABP1P2 and DmsEFAB/MtrCAB in iodate reduction.
  2. Exploration of Ecological Importance: The paper emphasizes the ecological importance of bacteria in the global iodine cycle, particularly in marine and groundwater systems.
  3. Identification of Knowledge Gaps: The paper identifies critical knowledge gaps in current research, providing direction for future studies.

Conclusion

Bacteria play a crucial role in the global biogeochemical cycling of iodine through various pathways, including iodate reduction, iodide oxidation and accumulation, and organic iodine formation. This paper reviews recent advances in understanding the molecular mechanisms of bacterial-mediated iodine transformations and highlights critical knowledge gaps in current research. Future studies should further explore these questions to enhance our understanding of the global iodine cycle and develop models for predicting the biogeochemical fate and transport of 129I in contaminated sites.