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Girguis, P.

Publications and source records attributed to Girguis, P..

7 recordsLinked to original sources

Microbial Growth in an Enceladus Ocean Analog Medium Informed by Mineral Stability Modeling

Evidence from the Cassini mission confirmed that Saturns moon Enceladus hosts a subsurface alkaline ocean where rock-water reactions may generate redox disequilibria capable of supporting microbial metabolisms. To investigate potential microbial survival under simulated Enceladus ocean conditions, we used thermodynamic modeling to develop a salt formulation consistent with one possible Enceladus ocean composition and supplemented it with putative microbial energy sources to create a growth medium. The medium was inoculated with samples from diverse ocean world analog environments on Earth to determine which microorganisms could persist under Enceladus-like conditions. The microorganisms persisting in this geochemically bounded medium were heterotrophic, metabolically versatile bacteria with low carbon requirements. Genomic and physiological analyses further showed the presence of multiple stress-response pathways, sodium-based bioenergetic systems, osmoregulation strategies, and other adaptations consistent with survival in alkaline, low-nutrient settings. These results suggest that some stress-tolerant heterotrophic bacteria may serve as useful model organisms for life in Enceladus subsurface ocean. These findings demonstrate the value of geochemically modeled media as a framework for constraining habitability, identifying relevant biosignatures, and probing potential microbial survival strategies beyond Earth.

microbiology↗

Microbial Communities in Mesopelagic Fish Guts Suggest an Overlooked Component of Marine Biogeochemical Cycles

Each night, gigatons of oceanic midwater fishes participate in the largest vertical migration on Earth. This movement of organisms from the meso-to the epipelagic and back plays a major role in the flux of organic matter from the surface to the deep sea (the "biological pump"). To date studies have considered the role of fish exports in ocean biogeochemical cycles, but mesopelagic fish gut microbiomes are unquantified and likely play a role in metabolic transformations that influence these cycles. Here, we present data on the abundance of mesopelagic fish gut microbial communities and their functional potential to shape key chemical transformations. Our flow cytometric data from a diversity of taxa reveal that the density of microbes in mesopelagic fish guts is between 106-107 microbes ml-1: two to three orders of magnitude higher than the surrounding seawater. In light of the total estimated number of mesopelagic fishes, there are approximately 2.4x1020 -1.34x1024 gut prokaryotes in total, which without consideration of other biomass abundant animals is realistically within four orders of magnitude of the total prokaryote abundance in mesopelagic waters. Metagenomic analyses revealed distinct bacterial genotypes of the genera Acinetobacter and Psychrobacter that harbor extensive gene sets for synthesis of essential amino acids, cofactor and vitamins, and short-chain-fatty acids (SCFAs), as well as cellulose and chitin degradation. Given their abundance, mesopelagic fish gut microbiomes are likely playing a role in shaping the nitrogen and carbon cycles, including through calcium carbonate precipitation and sequestration. Moreover, gut microbes are likely more metabolically active than bacterioplankton given that animals actively feed and accumulate organic matter amongst co-concentrated microbes. Gut microbes, especially if we consider all epi-to bathypelagic animals, may represent a significant and previously unrecognized component of marine biogeochemical cycles, though their relative importance compared to free-living microbes requires further quantification. Significance StatementThe daily vertical migration of oceanic midwater fishes represents Earths largest animal migration and facilitates the transfer of nutrients from surface to deep waters. Despite their critical role in shaping ocean biogeochemistry, the gut microbiomes of these fishes have remained largely uncharacterized. We demonstrate that mesopelagic fishes harbor dense gut microbial communities -two to three orders of magnitude higher than surrounding seawater-that collectively may be within four orders of magnitude of the total prokaryote abundance in global mesopelagic waters. These gut microbes possess extensive metabolic capabilities for nutrient cycling and likely shape the prevailing biogeochemical and microbial ecological processes in the water column. Given the high likelihood that gut microbes are more metabolically active than free-living bacterioplankton, our findings reveal a previously unrecognized biological component that may fundamentally shape marine biogeochemical cycles and global carbon sequestration.

microbiology↗

Humpback whales harbor a highly novel and endemic gut microbiome that adapts to periods of fasting during migration

Humpback whales (Megaptera novaeangliae) are cosmopolitan in distribution and most populations migrate between foraging and breeding grounds each year1,2. As capital breeders, many humpbacks reduce foraging behavior and potentially fast for a few months of the year3. Here, we present a comparative genomic analysis of the gut microbiomes from humpbacks on two breeding grounds: Gulf of California, where feeding is common4-6, and Hawai i, where feeding is extremely rare7. The humpback whale gut microbiome shows unexpected taxonomic novelty, high endemism, and coevolutionary signal. These data also suggest an imbalance in the gut community with foraging reduction, supported by the enrichment of several aerobic metabolism genes, potentially indicative of inflammation, and pathogenesis gene sets used to colonize host tissues, modulate the immune system, and lyse tissues. Pathway reconstruction revealed gut communities shared symbiotic functions including the synthesis of essential amino acids, short chain fatty acids (SCFAs), and vitamins, as well as nitrogen salvaging mechanisms and degradation of biogeochemically relevant substrates like cellulose, chitin, and wax esters (including host chitinases). Complementary sequencing and taxonomic annotation revealed that more Clostridiaceae and Oscillospiraceae genera were in foraging whales, whereas fasting samples were enriched in Erysipelotrichaceae genera, associated with gut disease8,9. These data reveal striking changes in humpback whale gut microbiomes between their feeding and breeding grounds, raise the possibility that breeding whales are more susceptible to gut dysfunction or disease, and equally important reveal how humpback whales are likely making varying biogeochemical contributions to upper ocean communities over the course of the year.

genomics↗

Deep learning of genomic contexts predicts protein co-regulation and function

Deciphering the relationship between a gene and its genomic context is fundamental to understanding and engineering biological systems. Machine learning has shown promise in learning latent relationships underlying the sequence-structure-function paradigm from massive protein sequence datasets. However, to date, limited attempts have been made in extending this continuum to include higher order genomic context information. Evolutionary processes dictate the specificity of genomic contexts in which a gene is found across phylogenetic distances, and these emergent genomic patterns can be leveraged to uncover functional relationships between gene products. Here, we trained a genomic language model (gLM) on millions of metagenomic scaffolds to learn the latent functional and regulatory relationships between genes. gLM learns contextualized protein embeddings that capture the genomic context as well as the protein sequence itself, and encode biologically meaningful and functionally relevant information (e.g. enzymatic function, taxonomy). Our analysis of the attention patterns demonstrates that gLM is learning co-regulated functional modules (i.e. operons). Our findings illustrate that gLMs unsupervised deep learning of the metagenomic corpus is an effective and promising approach to encode functional semantics and regulatory syntax of genes in their genomic contexts and uncover complex relationships between genes in a genomic region.

bioinformatics↗

Novel insights on obligate symbiont lifestyle and adaptation to chemosynthetic environment as revealed by the giant tubeworm genome

The mutualism between the giant tubeworm Riftia pachyptila and its endosymbiont Candidatus Endoriftia persephone has been extensively researched over the past 40 years. However, the lack of the host whole genome information has impeded the full comprehension of the genotype/phenotype interface in Riftia. Here we described the high-quality draft genome of Riftia, its complete mitogenome, and tissue-specific transcriptomic data. The Riftia genome presents signs of reductive evolution, with gene family contractions exceeding expansions. Expanded gene families are related to sulphur metabolism, detoxification, anti-oxidative stress, oxygen transport, immune system, and lysosomal digestion, reflecting evolutionary adaptations to the vent environment and endosymbiosis. Despite the derived body plan, the developmental gene repertoire in the gutless tubeworm is extremely conserved with the presence of a near intact and complete Hox cluster. Gene expression analyses establishes that the trophosome is a multi-functional organ marked by intracellular digestion of endosymbionts, storage of excretory products and haematopoietic functions. Overall, the plume and gonad tissues both in contact to the environment harbour highly expressed genes involved with cell cycle, programmed cell death, and immunity indicating a high cell turnover and defence mechanisms against pathogens. We posit that the innate immune system plays a more prominent role into the establishment of the symbiosis during the infection in the larval stage, rather than maintaining the symbiostasis in the trophosome. This genome bridges four decades of physiological research in Riftia, whilst simultaneously provides new insights into the development, whole organism functions and evolution in the giant tubeworm.

evolutionary biology↗

Spatially-resolved correlative microscopy and microbial identification reveals dynamic depth- and mineral-dependent anabolic activity in salt marsh sediment

Coastal salt marshes are key sites of biogeochemical cycling and ideal systems in which to investigate the community structure of complex microbial communities. Here, we clarify structural-functional relationships among microorganisms and their mineralogical environment, revealing previously undescribed metabolic activity patterns and precise spatial arrangements within salt marsh sediment. Following 3.7-day in situ incubations with a non-canonical amino acid that was incorporated into new biomass, samples were embedded and analyzed by correlative fluorescence and electron microscopy to map the microscale arrangements of anabolically active and inactive organisms alongside mineral grains. Parallel sediment samples were examined by fluorescence-activated cell sorting and 16S rRNA gene sequencing to link anabolic activity to taxonomic identity. Both approaches demonstrated a rapid decline in the proportion of anabolically active cells with depth into salt marsh sediment, from [~]60% in the top cm to 10-25% between 2-7 cm. From the top to the bottom, the most prominent active community members shifted from sulfur cycling phototrophic consortia, to sulfate-reducing bacteria likely oxidizing organic compounds, to fermentative lineages. Correlative microscopy revealed more abundant (and more anabolically active) organisms around non-quartz minerals including rutile, orthoclase, and plagioclase. Microbe-mineral relationships appear to be dynamic and context-dependent arbiters of biogeochemical cycling. Statement of SignificanceMicroscale spatial relationships dictate critical aspects of a microbiomes inner workings and emergent properties, such as evolutionary pathways, niche development, and community structure and function. However, many commonly used methods in microbial ecology neglect this parameter - obscuring important microbe-microbe and microbe-mineral interactions - and instead employ bulk-scale methodologies that are incapable of resolving these intricate relationships. This benchmark study presents a compelling new approach for exploring the anabolic activity of a complex microbial community by mapping the precise spatial configuration of anabolically active organisms within mineralogically heterogeneous sediment through in situ incubation, resin embedding, and correlative fluorescence and electron microscopy. In parallel, active organisms were identified through fluorescence-activated cell sorting and 16S rRNA gene sequencing, enabling a powerful interpretive framework connecting location, identity, activity, and putative biogeochemical roles of microbial community members. We deploy this novel approach in salt marsh sediment, revealing quantitative insights into the fundamental principles that govern the structure and function of sediment-hosted microbial communities. In particular, at different sediment horizons, we observed striking changes in the proportion of anabolically active cells, the identities of the most prominent active community members, and the nature of microbe-mineral affiliations. Improved approaches for understanding microscale ecosystems in a new light, such as those presented here, reveal environmental parameters that promote or constrain metabolic activity and clarify the impact that microbial communities have on our world.

microbiology↗

Methane-linked mechanisms of electron uptake from cathodes by Methanosarcina barkeri

The Methanosarcinales, a lineage of cytochrome-containing methanogens, have recently been proposed to participate in direct extracellular electron transfer interactions within syntrophic communities. To shed light on this phenomenon, we applied electrochemical techniques to measure electron uptake from cathodes by Methanosarcina barkeri, which is an important model organism that is genetically tractable and utilizes a wide range of substrates for methanogenesis. Here we confirm the ability of M. barkeri to perform electron uptake from cathodes and show that this cathodic current is linked to quantitative increases in methane production. The underlying mechanisms we identified include, but are not limited to, a recently proposed association between cathodes and methanogen-derived extracellular enzymes (e.g. hydrogenases) that can facilitate current generation through the formation of reduced and diffusible methanogenic substrates (e.g. hydrogen). However, after minimizing the contributions of such extracellular enzymes and using a mutant lacking hydrogenases, we observe a lower potential hydrogen-independent pathway that facilitates cathodic activity coupled to methane production in M. barkeri. Our electrochemical measurements of wild-type and mutant strains point to a novel and extracellular-enzyme-free mode of electron uptake able to take up electrons at potentials lower than - 498 mV vs. SHE (over 100 mV more reduced than the observed hydrogenase midpoint potential under these conditions). These results suggest that M. barkeri can perform multiple modes (hydrogenase-mediated and free extracellular enzyme-independent) of electrode interactions on cathodes including a mechanism pointing to a direct interaction, which has significant applied and ecological implications.\n\nImportanceMethanogenic Archaea are of fundamental applied and environmental relevance. This is largely due to their activities in a wide range of anaerobic environments, generating gaseous reduced carbon that can be utilized as a fuel source. While the bioenergetics of a wide variety of methanogens has been well studied with respect to soluble substrates, mechanistic understanding of their interaction with solid phase redox active compounds is limited. This work provides insight into solid phase redox interactions in Methanosarcina using electrochemical methods. We highlight a previously undescribed mode of electron uptake from cathodes, that is potentially informative of direct interspecies electron transfer interactions in the Methanosarcinales.

microbiology↗