Environmental Breviatea harbour mutualistic Arcobacter epibionts.

Breviatea form a lineage of free living, unicellular protists, distantly related to animals and fungi. This lineage emerged almost one billion years ago, when the oceanic oxygen content was low, and extant Breviatea have evolved or retained an anaerobic lifestyle. Here we report the cultivation of Lenisia limosa, gen. et sp. nov., a newly discovered breviate colonized by relatives of animal-associated Arcobacter. Physiological experiments show that the association of L. limosa with Arcobacter is driven by the transfer of hydrogen and is mutualistic, providing benefits to both partners. With whole-genome sequencing and differential proteomics, we show that an experimentally observed fitness gain of L. limosa could be explained by the activity of a so far unknown type of NAD(P)H-accepting hydrogenase, which is expressed in the presence, but not in the absence, of Arcobacter. Differential proteomics further reveal that the presence of Lenisia stimulates expression of known 'virulence' factors by Arcobacter. These proteins typically enable colonization of animal cells during infection, but may in the present case act for mutual benefit. Finally, re-investigation of two currently available transcriptomic data sets of other Breviatea reveals the presence and activity of related hydrogen-consuming Arcobacter, indicating that mutualistic interaction between these two groups of microbes might be pervasive. Our results support the notion that molecular mechanisms involved in virulence can also support mutualism, as shown here for Arcobacter and Breviatea.

Temperature limits to deep subseafloor life in the Nankai Trough subduction zone.

Microorganisms in marine subsurface sediments substantially contribute to global biomass. Sediments warmer than 40°C account for roughly half the marine sediment volume, but the processes mediated by microbial populations in these hard-to-access environments are poorly understood. We investigated microbial life in up to 1.2-kilometer-deep and up to 120°C hot sediments in the Nankai Trough subduction zone. Above 45°C, concentrations of vegetative cells drop two orders of magnitude and endospores become more than 6000 times more abundant than vegetative cells. Methane is biologically produced and oxidized until sediments reach 80° to 85°C. In 100° to 120°C sediments, isotopic evidence and increased cell concentrations demonstrate the activity of acetate-degrading hyperthermophiles. Above 45°C, populated zones alternate with zones up to 192 meters thick where microbes were undetectable.

Microbial dormancy in the marine subsurface: Global endospore abundance and response to burial.

Marine sediments host an unexpectedly large microbial biosphere, suggesting unique microbial mechanisms for surviving burial and slow metabolic turnover. Although dormancy is generally considered an important survival strategy, its specific role in subsurface sediments remains unclear. We quantified dormant bacterial endospores in 331 marine sediment samples from diverse depositional types and geographical origins. The abundance of endospores relative to vegetative cells increased with burial depth and endospores became dominant below 25 m, with an estimated population of 2.5 × 1028 to 1.9 × 1029 endospores in the uppermost kilometer of sediment and a corresponding biomass carbon of 4.6 to 35 Pg surpassing that of vegetative cells. Our data further identify distinct endospore subgroups with divergent resistance to burial and aging. Endospores may shape the deep biosphere by providing a core population for colonization of new habitats and/or through low-frequency germination to sustain slow growth in this environment.

Carbon flow from volcanic CO2 into soil microbial communities of a wetland mofette.

Effects of extremely high carbon dioxide (CO2) concentrations on soil microbial communities and associated processes are largely unknown. We studied a wetland area affected by spots of subcrustal CO2 degassing (mofettes) with focus on anaerobic autotrophic methanogenesis and acetogenesis because the pore gas phase was largely hypoxic. Compared with a reference soil, the mofette was more acidic (ΔpH ∼0.8), strongly enriched in organic carbon (up to 10 times), and exhibited lower prokaryotic diversity. It was dominated by methanogens and subdivision 1 Acidobacteria, which likely thrived under stable hypoxia and acidic pH. Anoxic incubations revealed enhanced formation of acetate and methane (CH4) from hydrogen (H2) and CO2 consistent with elevated CH4 and acetate levels in the mofette soil. (13)CO2 mofette soil incubations showed high label incorporations with ∼512 ng (13)C g (dry weight (dw)) soil(-1) d(-1) into the bulk soil and up to 10.7 ng (13)C g (dw) soil(-1) d(-1) into almost all analyzed bacterial lipids. Incorporation of CO2-derived carbon into archaeal lipids was much lower and restricted to the first 10 cm of the soil. DNA-SIP analysis revealed that acidophilic methanogens affiliated with Methanoregulaceae and hitherto unknown acetogens appeared to be involved in the chemolithoautotrophic utilization of (13)CO2. Subdivision 1 Acidobacteriaceae assimilated (13)CO2 likely via anaplerotic reactions because Acidobacteriaceae are not known to harbor enzymatic pathways for autotrophic CO2 assimilation. We conclude that CO2-induced geochemical changes promoted anaerobic and acidophilic organisms and altered carbon turnover in affected soils.

Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface.

Subsurface microbial life contributes significantly to biogeochemical cycling, yet it remains largely uncharacterized, especially its archaeal members. This 'microbial dark matter' has been explored by recent studies that were, however, mostly based on DNA sequence information only. Here, we use diverse techniques including ultrastuctural analyses to link genomics to biology for the SM1 Euryarchaeon lineage, an uncultivated group of subsurface archaea. Phylogenomic analyses reveal this lineage to belong to a widespread group of archaea that we propose to classify as a new euryarchaeal order ('Candidatus Altiarchaeales'). The representative, double-membraned species 'Candidatus Altiarchaeum hamiconexum' has an autotrophic metabolism that uses a not-yet-reported Factor420-free reductive acetyl-CoA pathway, confirmed by stable carbon isotopic measurements of archaeal lipids. Our results indicate that this lineage has evolved specific metabolic and structural features like nano-grappling hooks empowering this widely distributed archaeon to predominate anaerobic groundwater, where it may represent an important carbon dioxide sink.