Ecological and genomic attributes of novel bacterial taxa that thrive in subsurface soil horizons

Brewer, Tess E.; Aronson, Emma L.; Arogyaswamy, Keshav; Billings, S. A.; Botthoff, Jon; Campbell, Ashley; Dove, Nicholas C.; Fairbanks, Dawson; Gallery, Rachel E.; Hart, Stephen C.; Kaye, Jason P.; King, Gary M.; Logan, Geoffrey D.; Lohse, Kathleen A.; Maltz, Mia R.; Mayorga, Emilio; O’Neill, Caitlin; Owens, Sarah M.; Packman, Aaron I.; Pett‐Ridge, Jennifer; Plante, Alain F.; Richter, Daniel D.; Silver, Whendee L.; Yang, Wendy H.; Fierer, Noah

doi:10.1101/647651

Cited by 9 publications

(17 citation statements)

References 62 publications

(61 reference statements)

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“…Here, our data of 16S rRNA gene sequences showed that Anaerolinea steadily increased from 0.001% in the surface organic layer to 0.009% in the middle organic layer, 0.011% in the deep organic layer, and 1.162% in the mineral layer, despite the insignificant difference between warmed and control plots in this study. Interestingly, the phylum Dormibacteraeota , which has no cultured representatives so far (Brewer et al, 2019), was abundant in subsurface soils. As Dormibacteraeota appears to adapt to cold and C‐depleted environments (Costello, 2007), it might be used as a bioindicator of cold soils because it is highly abundant in much permafrost of Alaska (Tas et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Permafrost thaw with warming reduces microbial metabolic capacities in subsurface soils

Yang

Feng

et al. 2021

Molecular Ecology

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Microorganisms are major constituents of the total biomass in permafrost regions, whose underlain soils are frozen for at least two consecutive years. To understand potential microbial responses to climate change, here we examined microbial community compositions and functional capacities across four soil depths in an Alaska tundra site. We showed that a 5-year warming treatment increased soil thaw depth by 25.7% (p = .011) within the deep organic layer (15-25 cm). Concurrently, warming reduced 37% of bacterial abundance and 64% of fungal abundances in the deep organic layer, while it did not affect microbial abundance in other soil layers (i.e., 0-5, 5-15, and 45-55 cm). Warming treatment altered fungal community composition and microbial functional structure (p < .050), but not bacterial community composition. Using a functional gene array, we found that the relative abundances of a variety of carbon (C)-decomposing, iron-reducing, and sulphate-reducing genes in the deep organic layer were decreased, which was not observed by the shotgun sequencing-based metagenomics analysis of those samples. To explain the reduced metabolic capacities, we found that warming treatment elicited higher deterministic environmental filtering, which could be linked to water-saturated time, soil moisture, and soil thaw duration. In contrast, plant factors showed little influence on microbial communities in subsurface soils below 15 cm, despite a 25.2% higher (p < .05) aboveground plant biomass by warming treatment. Collectively, we demonstrate that microbial metabolic capacities in subsurface soils are reduced, probably arising from enhanced thaw by warming.

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Section: Discussionmentioning

confidence: 99%

Permafrost thaw with warming reduces microbial metabolic capacities in subsurface soils

Yang

Feng

et al. 2021

Molecular Ecology

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“…Ca . Dormibacterota have been reported to be more abundant in low carbon (Brewer et al ., 2019), or low nitrogen environments (Tas et al ., 2014), with an increase in abundance with depth of sampling reported (Tas et al ., 2014; Woodcroft et al ., 2018; Brewer et al ., 2019). For example, Ca .…”

Section: Introductionmentioning

confidence: 99%

“…For example, Ca . Dormibacterota have been shown to increase 27‐fold in relative abundance at a sampling depth of 90 cm in sub‐surface soil horizons in North American forest soils, representing up to 60% relative abundance in these nutrient‐depleted soils (Brewer et al ., 2019).…”

Section: Introductionmentioning

confidence: 99%

Persistence and resistance: survival mechanisms of Candidatus Dormibacterota from nutrient‐poor Antarctic soils

Montgomery

Williams

Brettle

et al. 2021

Environmental Microbiology

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Summary Candidatus Dormibacterota is an uncultured bacterial phylum found predominantly in soil that is present in high abundances within cold desert soils. Here, we interrogate nine metagenome‐assembled genomes (MAGs), including six new MAGs derived from soil metagenomes obtained from two eastern Antarctic sites. Phylogenomic and taxonomic analyses revealed these MAGs represent four genera and five species, representing two order‐level clades within Ca. Dormibacterota. Metabolic reconstructions of these MAGs revealed the potential for aerobic metabolism, and versatile adaptations enabling persistence in the ‘extreme’ Antarctic environment. Primary amongst these adaptations were abilities to scavenge atmospheric H2 and CO as energy sources, as well as using the energy derived from H2 oxidation to fix atmospheric CO2 via the Calvin–Bassham–Benson cycle, using a RuBisCO type IE. We propose that these allow Ca. Dormibacterota to persist using H2 oxidation and grow using atmospheric chemosynthesis in terrestrial Antarctica. Fluorescence in situ hybridization revealed Ca. Dormibacterota to be coccoid cells, 0.3–1.4 μm in diameter, with some cells exhibiting the potential for a symbiotic or syntrophic lifestyle.

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“…Soil pH may also increase with depth in instances where the parent material is enriched in base cations (Brubaker et al 1993). These gradients in soil properties result in subsoil microbial communities that are vastly different than their surface soil counterparts (Eilers et al 2012;Brewer et al 2019). Soil pH (Sinsabaugh et al 2008;Kivlin & Treseder 2014), substrate availability and demand (Olander & Vitousek 2000;Doveet al 2019), and microbial community composition (Schneckeret al 2015) influence EE activities in surface soils.…”

Section: Introductionmentioning

confidence: 99%

“…However, it is currently unknown if these controls in surface soils extend into the subsoil. We posit that EE activities at depth may follow different patterns than in the surface horizons given that EEs at depth are less responsive to environmental perturbations (Jing et al 2017), subsoils have greater heterogeneity of organic substrates than at the surface (Salomé et al 2010), and the microbial communities at depth are dominated by oligotrophic microorganisms (Brewer et al 2019).…”

Section: Introductionmentioning

confidence: 99%

Continental-scale patterns of extracellular enzyme activity in the subsoil: an overlooked reservoir of microbial activity

et al.

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Stabilization of microbial-derived products such as extracellular enzymes (EE) has gained attention as a possibly important mechanism leading to the persistence of soil organic carbon (SOC). While the controls on EE activities and their stabilization in the surface soil are reasonably well-understood, how these activities change with soil depth and possibly diverge from those at the soil surface due to distinct physical, chemical, and biotic conditions remains unclear. We assessed EE activity to a depth of 1 m (10 cm increments) in 19 soil profiles across the Critical Zone Observatory Network, which represents a wide range of climates, soil orders, and vegetation types. Activities of four carbon (C)-acquiring enzymes (α-glucosidase, β-glucosidase, βxylosidase, and cellobiohydrolase), two nitrogen (N)-acquiring enzymes (N-acetylglucosaminidase and leucine aminopeptidase), and one phosphorus (P)-acquiring enzyme (acid phosphatase) were measured fluorometrically along with SOC, total N, Olsen P, pH, clay concentration, and phospholipid fatty acids, which we used to characterize the microbial community composition and biomass (MB). For all EEs, activities per gram soil correlated positively with MB and SOC; all of which decreased logarithmically with depth (p < 0.05). Across all sites, over half of the potential soil EE activities per gram soil consistently occurred below 20 cm for all measured EEs. Activities per unit MB or SOC were substantially higher at depth (soils below 20 cm accounted for 80% of whole-profile EE activity), suggesting an accumulation of stabilized (i.e., mineral sorbed) EEs in subsoil horizons. The pronounced enzyme stabilization in subsurface horizons was corroborated by mixed-effects models that showed a significant, positive relationship between clay concentration and MB-normalized EE activities in the subsoil. Furthermore, the negative relationships between soil C, N, and P and C-, N-, and P-acquiring EEs found in the surface soil decoupled at 20 cm, which could have also been caused by EE stabilization. This suggesting that EEs do not reflect soil nutrient availabilities at depth. Taken together, our results suggest that deeper soil horizons hold a significant reservoir of EEs, and that the controls of subsoil 1

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Ecological and genomic attributes of novel bacterial taxa that thrive in subsurface soil horizons

Abstract: While most bacterial and archaeal taxa living in surface soils remain undescribed, 5this problem is exacerbated in deeper soils owing to the unique oligotrophic conditions found in the subsurface.

Cited by 9 publications

References 62 publications

Permafrost thaw with warming reduces microbial metabolic capacities in subsurface soils

Permafrost thaw with warming reduces microbial metabolic capacities in subsurface soils

Persistence and resistance: survival mechanisms of Candidatus Dormibacterota from nutrient‐poor Antarctic soils

Continental-scale patterns of extracellular enzyme activity in the subsoil: an overlooked reservoir of microbial activity

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