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1. Population ecology and potential biogeochemical impacts of ssDNA and dsDNA soil viruses along a permafrost thaw gradient

   https://doi.org/10.1101/2023.06.13.544858  

   Trubl, Gareth; Roux, Simon; Borton, Mikayla A; Varsani, Arvind; Li, Yueh-Fen; Sun, Christine; Jang, Ho Bin; Woodcroft, Ben J; Tyson, Gene W; Wrighton, Kelly C; et al (June 2023, bioRxiv)

   Abstract Climate change is disproportionately warming northern peatlands, which may release large carbon stores via increased microbial activity. While there are many unknowns about such microbial responses, virus roles are especially poorly characterized with studies to date largely restricted to “bycatch” from bulk metagenomes. Here, we used optimized viral particle purification techniques on 20 samples along a highly contextualized peatland permafrost thaw gradient, extracted and sequenced viral particle DNA using two library kits to capture single-stranded (ssDNA) and double-stranded (dsDNA) virus genomes (40 total viromes), and explored their diversity and potential ecosystem impacts. Both kits recovered similar dsDNA virus numbers, but only one also captured thousands of ssDNA viruses. Combining these data, we explored population-level ecology using genomic representation from 9,560 viral operational taxonomic units (vOTUs); nearly a 4-fold expansion from permafrost-associated soils, and 97% of which were novel when compared against large datasets from soils, oceans, and the human gut.In silicopredictions identified putative hosts for 44% (4,149 dsDNA + 17 ssDNA) of the identified vOTUs spanning 2 eukaryotic, 12 archaeal, and 30 bacterial phyla. The recovered vOTUs encoded 1,684 putative auxiliary metabolic genes (AMGs) and other metabolic genes carried by ∼10% of detected vOTUs, of which 46% were related to carbon processing and 644 were novel. These AMGs grouped into five functional categories and 11 subcategories, and nearly half (47%) of the AMGs were involved in carbon utilization. Of these, 112 vOTUs encoded 123 glycoside hydrolases spanning 15 types involved in the degradation of polysaccharides (e.g., cellulose) to monosaccharides (e.g., galactose), or further monosaccharide degradation, which suggests virus involvement in myriad metabolisms including fermentation and central carbon metabolism. These findings expand the scope of viral roles in microbial carbon processing and suggest viruses may be critical for understanding the fate of soil organic carbon in peatlands. 

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2. Abrupt permafrost thaw drives spatially heterogeneous soil moisture and carbon dioxide fluxes in upland tundra

   https://doi.org/10.1111/gcb.16936  

   Rodenhizer, Heidi; Natali, Susan M.; Mauritz, Marguerite; Taylor, Meghan A.; Celis, Gerardo; Kadej, Stephanie; Kelley, Allison K.; Lathrop, Emma R.; Ledman, Justin; Pegoraro, Elaine F.; et al (November 2023, Global Change Biology)

   Abstract Permafrost thaw causes the seasonally thawed active layer to deepen, causing the Arctic to shift toward carbon release as soil organic matter becomes susceptible to decomposition. Ground subsidence initiated by ice loss can cause these soils to collapse abruptly, rapidly shifting soil moisture as microtopography changes and also accelerating carbon and nutrient mobilization. The uncertainty of soil moisture trajectories during thaw makes it difficult to predict the role of abrupt thaw in suppressing or exacerbating carbon losses. In this study, we investigated the role of shifting soil moisture conditions on carbon dioxide fluxes during a 13‐year permafrost warming experiment that exhibited abrupt thaw. Warming deepened the active layer differentially across treatments, leading to variable rates of subsidence and formation of thermokarst depressions. In turn, differential subsidence caused a gradient of moisture conditions, with some plots becoming consistently inundated with water within thermokarst depressions and others exhibiting generally dry, but more variable soil moisture conditions outside of thermokarst depressions. Experimentally induced permafrost thaw initially drove increasing rates of growing season gross primary productivity (GPP), ecosystem respiration (R_eco), and net ecosystem exchange (NEE) (higher carbon uptake), but the formation of thermokarst depressions began to reverse this trend with a high level of spatial heterogeneity. Plots that subsided at the slowest rate stayed relatively dry and supported higher CO₂fluxes throughout the 13‐year experiment, while plots that subsided very rapidly into the center of a thermokarst feature became consistently wet and experienced a rapid decline in growing season GPP,R_eco, and NEE (lower carbon uptake or carbon release). These findings indicate that Earth system models, which do not simulate subsidence and often predict drier active layer conditions, likely overestimate net growing season carbon uptake in abruptly thawing landscapes. 

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3. A global atlas of soil viruses reveals unexplored biodiversity and potential biogeochemical impacts

   https://doi.org/10.1038/s41564-024-01686-x  

   Graham, Emily B; Camargo, Antonio Pedro; Wu, Ruonan; Neches, Russell Y; Nolan, Matt; Paez-Espino, David; Kyrpides, Nikos C; Jansson, Janet K; McDermott, Jason E; Hofmockel, Kirsten S; et al (July 2024, Nature Microbiology)

   Abstract Historically neglected by microbial ecologists, soil viruses are now thought to be critical to global biogeochemical cycles. However, our understanding of their global distribution, activities and interactions with the soil microbiome remains limited. Here we present the Global Soil Virus Atlas, a comprehensive dataset compiled from 2,953 previously sequenced soil metagenomes and composed of 616,935 uncultivated viral genomes and 38,508 unique viral operational taxonomic units. Rarefaction curves from the Global Soil Virus Atlas indicate that most soil viral diversity remains unexplored, further underscored by high spatial turnover and low rates of shared viral operational taxonomic units across samples. By examining genes associated with biogeochemical functions, we also demonstrate the viral potential to impact soil carbon and nutrient cycling. This study represents an extensive characterization of soil viral diversity and provides a foundation for developing testable hypotheses regarding the role of the virosphere in the soil microbiome and global biogeochemistry. 

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4. Variability in above- and belowground carbon stocks in a Siberian larch watershed

   https://doi.org/10.5194/bg-14-4279-2017  

   Webb, Elizabeth E.; Heard, Kathryn; Natali, Susan M.; Bunn, Andrew G.; Alexander, Heather D.; Berner, Logan T.; Kholodov, Alexander; Loranty, Michael M.; Schade, John D.; Spektor, Valentin; et al (January 2017, Biogeosciences)

   null (Ed.)

   Abstract. Permafrost soils store between 1330 and 1580 Pg carbon (C), which is 3 times the amount of C in global vegetation, almost twice the amount of C in the atmosphere, and half of the global soil organic C pool. Despite the massive amount of C in permafrost, estimates of soil C storage in the high-latitude permafrost region are highly uncertain, primarily due to undersampling at all spatial scales; circumpolar soil C estimates lack sufficient continental spatial diversity, regional intensity, and replication at the field-site level. Siberian forests are particularly undersampled, yet the larch forests that dominate this region may store more than twice as much soil C as all other boreal forest types in the continuous permafrost zone combined. Here we present above- and belowground C stocks from 20 sites representing a gradient of stand age and structure in a larch watershed of the Kolyma River, near Chersky, Sakha Republic, Russia. We found that the majority of C stored in the top 1 m of the watershed was stored belowground (92 %), with 19 % in the top 10 cm of soil and 40 % in the top 30 cm. Carbon was more variable in surface soils (10 cm; coefficient of variation (CV)  =  0.35 between stands) than in the top 30 cm (CV  =  0.14) or soil profile to 1 m (CV  =  0.20). Combined active-layer and deep frozen deposits (surface – 15 m) contained 205 kg C m−2 (yedoma, non-ice wedge) and 331 kg C m−2 (alas), which, even when accounting for landscape-level ice content, is an order of magnitude more C than that stored in the top meter of soil and 2 orders of magnitude more C than in aboveground biomass. Aboveground biomass was composed of primarily larch (53 %) but also included understory vegetation (30 %), woody debris (11 %) and snag (6 %) biomass. While aboveground biomass contained relatively little (8 %) of the C stocks in the watershed, aboveground processes were linked to thaw depth and belowground C storage. Thaw depth was negatively related to stand age, and soil C density (top 10 cm) was positively related to soil moisture and negatively related to moss and lichen cover. These results suggest that, as the climate warms, changes in stand age and structure may be as important as direct climate effects on belowground environmental conditions and permafrost C vulnerability. 

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5. Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost

   https://doi.org/10.1128/msystems.00698-23  

   Ellenbogen, Jared B; Borton, Mikayla A; McGivern, Bridget B; Cronin, Dylan R; Hoyt, David W; Freire-Zapata, Viviana; McCalley, Carmody K; Varner, Ruth K; Crill, Patrick M; Wehr, Richard A; et al (January 2024, mSystems)

   Hernandez, Marcela (Ed.)

   ABSTRACT While wetlands are major sources of biogenic methane (CH₄), our understanding of resident microbial metabolism is incomplete, which compromises the prediction of CH₄emissions under ongoing climate change. Here, we employed genome-resolved multi-omics to expand our understanding of methanogenesis in the thawing permafrost peatland of Stordalen Mire in Arctic Sweden. In quadrupling the genomic representation of the site’s methanogens and examining their encoded metabolism, we revealed that nearly 20% of the metagenome-assembled genomes (MAGs) encoded the potential for methylotrophic methanogenesis. Further, 27% of the transcriptionally active methanogens expressed methylotrophic genes; forMethanosarcinalesandMethanobacterialesMAGs, these data indicated the use of methylated oxygen compounds (e.g., methanol), while forMethanomassiliicoccales, they primarily implicated methyl sulfides and methylamines. In addition to methanogenic methylotrophy, >1,700 bacterial MAGs across 19 phyla encoded anaerobic methylotrophic potential, with expression across 12 phyla. Metabolomic analyses revealed the presence of diverse methylated compounds in the Mire, including some known methylotrophic substrates. Active methylotrophy was observed across all stages of a permafrost thaw gradient in Stordalen, with the most frozen non-methanogenic palsa found to host bacterial methylotrophy and the partially thawed bog and fully thawed fen seen to house both methanogenic and bacterial methylotrophic activities. Methanogenesis across increasing permafrost thaw is thus revised from the sole dominance of hydrogenotrophic production and the appearance of acetoclastic at full thaw to consider the co-occurrence of methylotrophy throughout. Collectively, these findings indicate that methanogenic and bacterial methylotrophy may be an important and previously underappreciated component of carbon cycling and emissions in these rapidly changing wetland habitats. IMPORTANCEWetlands are the biggest natural source of atmospheric methane (CH₄) emissions, yet we have an incomplete understanding of the suite of microbial metabolism that results in CH₄formation. Specifically, methanogenesis from methylated compounds is excluded from all ecosystem models used to predict wetland contributions to the global CH₄budget. Though recent studies have shown methylotrophic methanogenesis to be active across wetlands, the broad climatic importance of the metabolism remains critically understudied. Further, some methylotrophic bacteria are known to produce methanogenic by-products like acetate, increasing the complexity of the microbial methylotrophic metabolic network. Prior studies of Stordalen Mire have suggested that methylotrophic methanogenesis is irrelevantin situand have not emphasized the bacterial capacity for metabolism, both of which we countered in this study. The importance of our findings lies in the significant advancement toward unraveling the broader impact of methylotrophs in wetland methanogenesis and, consequently, their contribution to the terrestrial global carbon cycle. 

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