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Morono, Y.

Publications and source records attributed to Morono, Y..

7 recordsLinked to original sources

Piezophilic activity dominates the Puerto Rico Trench deep subseafloor biosphere

Hydrostatic pressure is a defining feature of the deep ocean, yet how it structures microbial activity across the subseafloor biosphere is poorly understood. Here, we assess pressure effects on anabolic activity in seafloor and subseafloor communities across a margin-to-hadal-to-abyssal transect of the Puerto Rico Trench region (493-8,385 m water depth). Community-level responses to pressure reverse with burial, revealing a previously unrecognized shift toward piezophily in resident subseafloor communities down to 20 meters below seafloor (mbsf). In pressure-incubation experiments, atmospheric pressure yielded higher proportions of active cells in surficial sediments, whereas in situ pressure yielded higher proportions in the subseafloor. Pressure also structured active-community composition; in trench-axis sediments extending to 8.35 mbsf, JS1/Atribacterota populations belonging to geographically widespread hadal lineages exhibited a physiological response to in situ pressure, indicative of subseafloor piezophily. These findings suggest that hydrostatic pressure acts as an ecological filter after burial, favoring piezophilic traits that may support microbial persistence in the deep subseafloor biosphere.

microbiology↗

Eukaryotes' closest relatives are internally simple syntrophic archaea

Eukaryotes are theorized to have originated from an archaeal phylum Promethearchaeota (formerly Asgard archaea)1,2. The first cultured representatives revealed valuable insight3,4 but are distantly related to the first eukaryotic common ancestor (FECA), leaving many unknowns regarding this archaeons biology. Here, we report isolation of two strains belonging to the order proposed as FECAs closest relative, Hodarchaeales,5 as members of a pure co- and tri-culture with methanogenic partners. Both are obligately anaerobic, syntrophic, peptide-degrading, and mesophilic archaea that have simple internal cell structure and produce protrusions and vesicles, like Promethearchaeales3,4. All strains demonstrate behavior focused on cell construction rather than division, unlike typical prokaryotes6. Strain HC1 possesses genes associated with aerobic lifestyles but lacks complete pathways for aerobic respiration and co-cultures cannot grow under (micro)aerobic conditions, suggesting the genes support oxygen detoxification rather than respiration. Reflecting this, HC1 can survive and grow under microaerobic conditions only when aerobic organisms are present. Phylogenetic analyses indicate FECA may have possessed these genes and thus some aerotolerance. Physiological, genomic, and phylogenetic observations indicate FECA was a simple-celled anaerobic syntrophic peptide-degrading archaeon with a non-growth-centric lifestyle and potential adaptations towards an oxygenated planet--the archaea-eukaryote transition was steep in both cell structure and aerobiosis.

microbiology↗

The DNA event horizon in the Guaymas Basin subsurface biosphere: technical advances and re-defined limits in bulk extractions of nucleic acids from deep marine sediments

We compiled DNA and RNA isolation protocols for sediment bulk extraction and their yields from Guaymas Basin subsurface sediments, and evaluated their sensitivity for metagenomic and amplicon analyses of subsurface microbial communities. Guaymas Basin sediments present a challenge for DNA and RNA recovery due to high concentrations of hydrocarbons, steep thermal gradients and rapidly declining cell numbers downcore. Metagenomic library construction and sequencing was possible from as little as 0.2 to 0.5 ng DNA/cm3 sediment; PCR amplification of 16S rRNA genes required in most cases approx. 1-2 ng DNA/cm3 sediment. At in-situ temperatures of 50 to 60{degrees}C, decreasing DNA recovery leads to increasingly uncertain "hit or miss" outcomes and to failures for metagenomic and amplicon analyses. DNA concentration profiles show that, even before these hot temperatures are reached, relatively moderate temperatures have a major effect on microbial abundance and DNA yield. Comparison with cell count profiles shows that hydrothermal influence is reducing downcore cell densities by multiple orders of magnitude faster compared to non-hydrothermal sediments; this effect is also visible at relatively moderate temperatures. To an even greater degree than DNA, RNA recovery is highly sensitive to downcore increasing temperatures and decreasing cell numbers, and worked best for microbial communities in cool, relatively shallow subsurface sediments.

microbiology↗

Single-cell analysis reveals an active and heterotrophic microbiome in the Guaymas Basin deep subsurface with significant heterotrophic inorganic carbon fixation

The marine subsurface is a long-term sink of atmospheric carbon dioxide with significant implications for climate on geologic timescales. Subsurface microbial cells can either enhance or reduce the potential for the subsurface to sequester carbon, depending on their metabolic activity. However, the activity of subsurface microbes is rarely measured, leaving their role in biogeochemical cycling poorly characterized. Here, we used nanoscale secondary ion mass spectrometry to quantify anabolic activity in 3,203 individual cells from the thermally altered deep subsurface in the Guaymas Basin, Mexico (3-75 m below the seafloor, 0-14 C). We observed that a large majority of cells were active (83-100%), although rates of biomass generation were low, suggesting cellular maintenance rather than doubling. Mean single-cell activity decreased with increasing sediment depth and temperature, and was most strongly correlated with porewater sulfate concentrations. Intracommunity heterogeneity in cell-specific activity decreased with increasing sediment depth and age. Using a dual-isotope labelling approach we determined that all active cells analyzed at all depths were heterotrophic. We detected and quantified inorganic carbon assimilation by heterotrophs and found that it contributes on average at least 5% of total heterotrophic biomass carbon in this community. Our results therefore suggest that the deep marine biosphere at Guaymas Basin is largely active and contributes to subsurface carbon cycling primarily by assimilating organic carbon but also by mediating heterotrophic inorganic carbon fixation. Heterotrophic assimilation of inorganic carbon may be a small yet significant and widespread underappreciated source of labile carbon in the global subsurface. ImportanceThe global subsurface is the largest reservoir of microbial life on the planet yet remains poorly characterized. The activity of life in this realm has implications for long-term elemental cycling, particularly of carbon, as well as how life survives in extreme environments. Here, we recovered cells from the deep subsurface of the Guaymas Basin and investigated the level and distribution of activity, the physicochemical drivers of activity, and the relative significance of organic versus inorganic carbon to subsurface biomass. Using a sensitive single-cell assay we find that the majority of cells are active, that activity is likely driven by availability of energy, and that while organic carbon supplies most cellular carbon, inorganic carbon also contributes. We additionally find that the inorganic carbon assimilation observed was mediated by heterotrophs, not autotrophs, highlighting the importance of this often overlooked mode of carbon assimilation in the subsurface and beyond.

microbiology↗

Microbial abundance and diversity in 64-74 Ma subseafloor igneous basement from the Louisville Seamount Chain

The aquifer in subseafloor igneous basement is a massive, continuous microbial substrate, yet sparingly little is known about life in this habitat. The work to date has focused largely on describing microbial diversity in young basement (<10 Ma) at oceanic spreading regions and ridge flanks, where the basaltic crust is still porous and fluid flow through it is active. While the prevailing belief used to be that fluid flow through older parts of the seafloor was non-existent, recent heat flow models predict that fluid moves through subseafloor basement >65 Ma, and that seamounts can act as mid-plate conduits for fluids into and out of the subsurface aquifer in older crustal settings. Here we test the hypothesis that microbial life exists in subseafloor basement >65Ma using samples collected from the Louisville Seamount Chain via seafloor drilling. Cell biomass was heterogeneous in nature and ranged from below detection to [~]104 cells cm-3. Bacterial 16S rRNA genes from core samples and enrichment incubations are dominated by lineages putatively carrying out hydrocarbon oxidation and nitrogen, sulfur and metal redox processes. Samples from two different seamounts were statistically different, indicating some degree of biogeography. Archaea were not detected via quantitative polymerase chain reaction, indicating they are rare in the Louisville subsurface. Taken together, the data indicate that microbial life is indeed present in subseafloor igneous basement >65 Ma, which significantly expands the range of the subseafloor biosphere where microbial life is known to exist. Impact StatementThe aquifer in subseafloor igneous basement is the largest continuous microbial substrate on Earth, but it is difficult to access and therefore understudied. We here collected samples from the Louisville Seamount Chain using seafloor drilling to determine if microbial life exists in the >65 Ma subseafloor basement made at these seamounts. A low biomass environment dominated by Bacteria potentially capable of using the Fe and S inherent in subseafloor basalt was detected, including Bacteria that were revived in enrichment experiments. This discovery expands the range of seafloor where confirmed microbial life exists and indicates the interior of seamounts is habitable.

ecology↗

Metagenomic Profiles of Archaea and Bacteria within Thermal and Geochemical Gradients of the Guaymas Basin Deep Subsurface

While the temperature gradients of Earths crust and sediments are thought to delineate the downward extent and ultimate limits of the subsurface biosphere, the actual course of consecutively changing microbial communities and activities, from cool surficial sediments towards the deep, hot biosphere, remains to be charted. We used metagenomic and metatranscriptomic analyses of the hydrothermally heated, massive sediment layers of Guaymas Basin (Gulf of California, Mexico) to examine the environmental distribution and activity patterns of bacteria and archaea along thermal, geochemical and cell count gradients. Composition and distribution of MAGs, dominated by Chloroflexota and Thermoproteota, were shaped by biogeochemical parameters as long as temperatures remained moderate, but downcore increasing temperatures overrode other factors beyond ca. 45{degrees}C. Consistently, MAG genome size and diversity decreased with increasing temperature, indicating a conspicuous downcore winnowing of the subsurface biosphere. In contrast, specific archaeal MAGs within the Thermoproteota and Hadarchaeota increased in relative abundance and in recruitment of transcriptome reads towards deeper, hotter sediments, and mark the transition towards a distinct deep, hot biosphere.

bioinformatics↗

Isolation of an archaeon at the prokaryote-eukaryote interface

The origin of eukaryotes remains enigmatic. Current data suggests that eukaryotes may have risen from an archaeal lineage known as \"Asgard archaea\". Despite the eukaryote-like genomic features found in these archaea, the evolutionary transition from archaea to eukaryotes remains unclear due to the lack of cultured representatives and corresponding physiological insight. Here we report the decade-long isolation of a Lokiarchaeota-related Asgard archaeon from deep marine sediment. The archaeon, \"Candidatus Prometheoarchaeum syntrophicum strain MK-D1\", is an anaerobic, extremely slow-growing, small cocci ([~]550 nm), that degrades amino acids through syntrophy. Although eukaryote-like intracellular complexities have been proposed for Asgard archaea, the isolate has no visible organella-like structure. Ca. P. syntrophicum instead displays morphological complexity - unique long, and often, branching protrusions. Based on cultivation and genomics, we propose an \"Entangle-Engulf-Enslave (E3) model\" for eukaryogenesis through archaea-alphaproteobacteria symbiosis mediated by the physical complexities and metabolic dependency of the hosting archaeon.

microbiology↗