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.

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.

Even though thermophiles are best known from geothermal and other heated systems, numerous studies have demonstrated that they occur ubiquitously in mesothermal and permanently cold soils and sediments. Cultivation based studies of the latter have revealed that the thermophiles within them are mostly spore-forming members of the Firmicutes. Since the geographic distribution of spores is presumably unconstrained by transport through the atmosphere, similar communities (composition and diversity) of thermophiles might be expected to emerge in mesothermal habitats after they are heated. Alternatively, thermophiles might experience environmental selection before or after heating leading to divergent communities. After demonstrating the ubiquity of anaerobic thermophiles and CO uptake in a variety of mesothermal habitats and two hot springs, we used high throughput sequencing of 16S rRNA genes to assess the composition and diversity of populations that emerged after incubation at 60°C with or without headspace CO concentrations of 25%. Anaerobic Firmicutes dominated relative abundances at most sites but anaerobic thermophilic members of the Acidobacteria and Proteobacteria were also common. Nonetheless, compositions at the amplicon sequence variant (ASV) level varied among the sites with no convergence resulting from heating or CO addition as indicated by beta diversity analyses. The distinctions among thermophilic communities paralleled patterns observed for unheated “time zero” mesothermal soils and sediments. Occupancy analyses showed that the number of ASVs occupying each of n sites decreased unimodally with increasing n; no ASV occupied all 14 sites and only one each occupied 11 and 12 sites, while 69.3% of 1873 ASVs occupied just one site. Nonetheless, considerations of distances among the sites occupied by individual ASVs along with details of their distributions indicated that taxa were not dispersal limited but rather were constrained by environmental selection. This conclusion was supported by βMNTD and βNTI analyses, which showed dispersal limitation was only a minor contributor to taxon distributions.