Distribution, Diversity, and Biogeography of Anaerobic Carbon Monoxide Uptake by Microbial Communities in Soils and Sediments

Carbon monoxide (CO) is primarily known for being a toxic gas. However, CO is used by microorganisms as an electron or carbon source in a variety of respiratory processes. Different kinds of microorganisms utilize CO aerobically and anaerobically, using two distinct CO dehydrogenases (CODHs). Aerobes oxidize CO using a molybdenum-dependent dehydrogenase (Mo-CODH), while anaerobes utilize a nickel-dependent CO dehydrogenase (Ni-CODH). Studies of the biochemistry and microbiology of aerobic and anaerobic CO oxidation are extensive, but relatively little is known about the ecology of anaerobic CO oxidation. In an effort to test new hypotheses about the ecology of anaerobic CO oxidation, a series of studies was undertaken using diverse soils and sediments that provided novel insights about the activity and biogeography of the process, its temperature sensitivity, and the diversity of microbial communities that participate in anaerobic CO uptake. CO uptake assays used low (10 ppm) CO concentrations under aerobic and anaerobic conditions, and high (25%) CO concentrations under anaerobic conditions at 25 °C and 60 °C. Anaerobic CO uptake occurred across all sites with low CO concentrations, even in recent volcanic deposits. Anaerobic CO uptake at high concentrations exhibited more variability. However, anaerobic CO uptake occurred in mesothermal and psychrothermal sites as well as in hot spring systems, suggesting that this process occurs in a wider range of environments and across a broader temperature range than previously reported. Analyses of microbial communities based on 16S rRNA gene sequences reveal distinct responses to elevated temperature, but less of response to elevated CO concentrations. However, there were enriched taxa, including known and putative Ni-dependent CO oxidizers, suggesting that anaerobic CO oxidizers may be more diverse than previously imagined

Anaerobic carbon monoxide uptake by microbial communities in volcanic deposits at different stages of successional development on o‐yama volcano, Miyake‐jima, Japan

© 2020 by the authors. Licensee MDPI, Basel, Switzerland. Research on Kilauea and O‐yama Volcanoes has shown that microbial communities and their activities undergo major shifts in response to plant colonization and that molyb-denum‐dependent CO oxidizers (Mo‐COX) and their activities vary with vegetation and deposit age. Results reported here reveal that anaerobic CO oxidation attributed to nickel‐dependent CO oxidizers (Ni‐COX) also occurs in volcanic deposits that encompass different developmental stages. Ni‐COX at three distinct sites responded rapidly to anoxia and oxidized CO from initial concentrations of about 10 ppm to sub‐atmospheric levels. CO was also actively consumed at initial 25% concentrations and 25 °C, and during incubations at 60 °C; however, uptake under the latter conditions was largely confined to an 800‐year‐old forested site. Analyses of microbial communities based on 16S rRNA gene sequences in treatments with and without 25% CO incubated at 25 °C or 60 °C revealed distinct responses to temperature and CO among the sites and evidence for enrichment of known and potentially novel Ni‐COX. The results collectively show that CO uptake by volcanic deposits occurs under a wide range of conditions; that CO oxidizers in volcanic deposits may be more diverse than previously imagined; and that Ni‐dependent CO oxidizers might play previously unsuspected roles in microbial succession

Anaerobic Carbon Monoxide Uptake by Microbial Communities in Volcanic Deposits at Different Stages of Successional Development on O-yama Volcano, Miyake-jima, Japan

Research on Kilauea and O-yama Volcanoes has shown that microbial communities and their activities undergo major shifts in response to plant colonization and that molybdenum-dependent CO oxidizers (Mo-COX) and their activities vary with vegetation and deposit age. Results reported here reveal that anaerobic CO oxidation attributed to nickel-dependent CO oxidizers (Ni-COX) also occurs in volcanic deposits that encompass different developmental stages. Ni-COX at three distinct sites responded rapidly to anoxia and oxidized CO from initial concentrations of about 10 ppm to sub-atmospheric levels. CO was also actively consumed at initial 25% concentrations and 25 °C, and during incubations at 60 °C; however, uptake under the latter conditions was largely confined to an 800-year-old forested site. Analyses of microbial communities based on 16S rRNA gene sequences in treatments with and without 25% CO incubated at 25 °C or 60 °C revealed distinct responses to temperature and CO among the sites and evidence for enrichment of known and potentially novel Ni-COX. The results collectively show that CO uptake by volcanic deposits occurs under a wide range of conditions; that CO oxidizers in volcanic deposits may be more diverse than previously imagined; and that Ni-dependent CO oxidizers might play previously unsuspected roles in microbial succession

Putative Nickel-Dependent Anaerobic Carbon Monoxide Uptake Occurs Commonly in Soils and Sediments at Ambient Temperature and Might Contribute to Atmospheric and Sub-Atmospheric Carbon Monoxide Uptake During Anoxic Conditions

Carbon monoxide (CO) occurs naturally in the atmosphere where it plays a critical role in tropospheric chemistry. Atmospheric CO uptake by soils has been well documented as an important CO sink and has been attributed to a group of aerobic bacteria that possess a molybdenum-dependent CO dehydrogenase (Mo-CODH). CO can also be oxidized by obligate Ni-dependent anaerobes (Ni-COX) that possess nickel-dependent CODHs (Ni-CODH) but relatively little is known about their ecology or their potential to contribute to CO dynamics within soils and sediments or to soil-atmosphere CO exchanges. Results from a series of assays undertaken with diverse soils and sediments and CO concentrations of 10 ppm and 25% with incubation temperatures of 10, 25, and 60°C revealed anaerobic uptake rates with 10 ppm CO that were comparable to those measured under oxic conditions; further, anaerobic CO uptake occurred without a lag and at atmospheric and sub-atmospheric CO concentrations. Assays with 25% CO revealed previously undocumented activity at 10°C and showed extensive activity at 25°C. Results from prior studies with isolates and soils suggest that anaerobic uptake at both 10 ppm and 25% CO concentrations might be attributed to Ni-COX. Collectively the results considerably expand the ecological range for Ni-COX and indicate that they could play previously unsuspected roles in soil CO dynamics