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Nicolas, A. M.

Publications and source records attributed to Nicolas, A. M..

9 recordsLinked to original sources

Codon bias, nucleotide selection, and genome size predict in situ bacterial growth rate and transcription in rewetted soil

In soils, the first rain after a prolonged dry period greatly impacts soil microbial community function, yet we lack a full understanding of the genomic traits associated with the microbial response to rewetting. Genomic traits such as codon usage bias and genome size have been linked to bacterial growth in soils--however this is often through measurements in culture. Here, we used metagenome-assembled genomes in combination with metatranscriptomics and 18O- water stable isotope probing to track genomic traits associated with transcriptional activity and growth of soil microorganisms over the course of one week following rewetting of a grassland soil. We found that the codon bias in ribosomal protein genes was the strongest predictor of growth rate. We also observed higher growth rates in bacteria with smaller genomes, demonstrating that reduced genome size contributes to bacterial growth responses to sudden changes in water or nutrient availability--potentially explaining why smaller genomes are more prevalent in arid and carbon poor systems. High levels of codon bias corresponded to faster transcriptional upregulation of ribosomal protein genes. In early transcribing taxa, nucleotides requiring less energy to produce were more common at synonymous substitution sites--where nucleotide substitutions did not change the encoded amino acid. We found several of these relationships also existed within a phylum, suggesting that association between genomic traits and activity could be a generalized characteristic of soil bacteria. These results provide in situ evidence that following rewetting, certain genomic characteristics affect soil microbial growth rate and transcription, and points towards the fitness advantages that these traits might pose for bacteria under changing conditions in soil.

microbiology↗

Vitamin B12 variants structure soil microbial communities despite soil's vast reservoir of B12.

Soil microbial communities perform critical ecosystem services through the collective metabolic activities of numerous individual organisms. Most microbes use corrinoids, a structurally diverse family of cofactors related to vitamin B12. Corrinoid structure influences the growth of individual microbes, yet how these growth responses scale to the community level remains unknown. Analysis of metagenome-assembled genomes suggests corrinoids are supplied to the community by members of the archaeal and bacterial phyla Thermoproteota, Actinobacteria, and Proteobacteria. Corrinoids were found largely adhered to the soil matrix in a grassland soil, at levels exceeding those required by cultured bacteria. Enrichment cultures and soil microcosms seeded with different corrinoids showed distinct shifts in bacterial community composition, supporting the hypothesis that corrinoid structure can shape communities. Environmental context influenced both community and taxon-specific responses to specific corrinoids. These results implicate corrinoids as key determinants of soil microbiome structure and suggest that environmental micronutrient reservoirs promote community stability.

microbiology↗

Phylogenetic distribution and experimental characterization of corrinoid production and dependence in soil bacterial isolates

Soil microbial communities impact carbon sequestration and release, biogeochemical cycling, and agricultural yields. These global effects rely on metabolic interactions that modulate community composition and function. However, the physicochemical and taxonomic complexity of soil and the scarcity of available isolates for phenotypic testing are significant barriers to studying soil microbial interactions. Corrinoids--the vitamin B12 family of cofactors--are critical for microbial metabolism, yet they are synthesized by only a subset of microbiome members. Here, we evaluated corrinoid production and dependence in soil bacteria as a model to investigate the ecological roles of microbes involved in metabolic interactions. We isolated and characterized a taxonomically diverse collection of 161 soil bacteria from a single study site. Most corrinoid-dependent bacteria in the collection prefer B12 over other corrinoids, while all tested producers synthesize B12, indicating metabolic compatibility between producers and dependents in the collection. Furthermore, a subset of producers release B12 at levels sufficient to support dependent isolates in laboratory culture at estimated ratios of up to 1,000 dependents per producer. Within our isolate collection, we did not find strong phylogenetic patterns in corrinoid production or dependence. Upon investigating trends in the phylogenetic dispersion of corrinoid metabolism categories across sequenced bacteria from various environments, we found that these traits are conserved in 47 out of 85 genera. Together, these phenotypic and genomic results provide evidence for corrinoid-based metabolic interactions among bacteria and provide a framework for the study of nutrient-sharing ecological interactions in microbial communities.

microbiology↗

Large language models are universal biomedical simulators

Computational simulation of biological processes can be a valuable tool in accelerating biomedical research, but usually requires extensive domain knowledge and manual adaptation. Recently, large language models (LLMs) such as GPT-4 have proven surprisingly successful for a wide range of tasks by generating human language at a very large scale. Here we explore the potential of leveraging LLMs as simulators of biological systems. We establish proof-of-concept of a text-based simulator, SimulateGPT, that uses LLM reasoning. We demonstrate good prediction performance for various biomedical applications, without requiring explicit domain knowledge or manual tuning. LLMs thus enable a new class of versatile and broadly applicable biological simulators. This text-based simulation paradigm is well-suited for modeling and understanding complex living systems that are difficult to describe with physics-based first-principles simulation, but for which extensive knowledge and context is available as written text.

bioinformatics↗

Isotope-enrichment reveals active viruses follow microbial host dynamics during rewetting of a California grassland soil

Viruses are abundant, ubiquitous members of soil communities that kill microbial cells, but how they respond to perturbation of soil ecosystems is essentially unknown. Here, we investigated lineage-specific virus-host dynamics in grassland soil following "wet-up", when resident microbes are both resuscitated and lysed after a prolonged dry period. Quantitative isotope tracing, time-resolved metagenomics and viromic analyses indicated that dry soil held a diverse but low biomass reservoir of virions, of which only a subset thrived following wet-up. Viral richness decreased by 50% within 24 h post wet-up, while viral biomass increased four-fold within one week. Counter to recent hypotheses suggesting temperate viruses predominate in soil, our evidence indicates that wet-up is dominated by viruses in lytic cycles. We estimate that viruses drive a measurable and continuous rate of cell lysis, with up to 46% of microbial death driven by viral lysis one week following wet-up. Thus, viruses contribute to turnover of soil microbial biomass and the widely reported CO2 efflux following wet-up of seasonally dry soils.

microbiology↗

Functional succession of actively growing soil microorganisms during rewetting is shaped by precipitation history

Rewetting of seasonally dry soils induces a burst of microbial activity and carbon mineralization that changes nutrient availability and leads to succession. Yet the microbial functions that underpin this succession are not well described. Further, its unclear how previous precipitation frames microbial capacities after rewetting and how long these effects persist. We used isotopically-labeled water to rewet seasonally dry annual grassland soil that experienced either mean annual or reduced precipitation during the previous two years, and sampled at five subsequent time points. We used quantitative stable isotope probing (qSIP)-informed genome- resolved metagenomics to identify growing microorganisms, predict their capabilities, and analyze how these traits differed over time and between precipitation treatments. Organisms that grew after wetup were more abundant than non-growing organisms prior to the wet-up, suggesting that traits that initiate succession are pre-defined at the end of the prior plant growing season or via survival over the summer. Fast-growing organisms had fewer carbohydrate active enzyme (CAZy) genes per genome than slower-growing organisms, suggesting that although fast-growers were capable of degrading complex C, they may not specialize in this process. Differential abundance of CAZy genes in growing organisms throughout the succession implies that substrate availability varied with time. In contrast, the abundance of peptidases in growing organisms differed between precipitation treatments, but not over time following wet-up. Before wet-up, the soil organisms gene inventories were different between the two precipitation treatments. Surprisingly, this legacy effect waned after just one week. Thus, pre-wetup differences in microbial functional capacity converged shortly after rewetting.

microbiology↗

Methane-derived carbon flow through host-virus trophic networks in soil

The concentration of atmospheric methane continues to increase with microbial communities controlling soil-atmosphere fluxes. While there is substantial knowledge of the diversity and function of organisms regulating methane production and consumption, the frequency and impact of interactions with viruses on their activity in soil is unknown. Metagenomic sequencing of soil microbial communities has enabled identification of linkages between viruses and hosts. However, determining host-virus linkages through sequencing does not determine whether a virus or a host are active. In this study, we identified active individual interactions in situ by following the transfer of assimilated carbon from active hosts to viruses. Using DNA stable-isotope probing combined with metagenomic analyses, we characterized methane-fueled microbial networks in acidic and neutral pH soils, specifically primary and secondary utilisers of carbon, together with the recent transfer of methane-derived carbon to viruses. Sixty-three percent of viral contigs from replicated soil incubations contained genes associated with known methanotrophic bacteria. Genomic sequences from 13C-enriched viruses were present in clustered regularly interspaced short palindromic repeats (CRISPR) arrays of multiple, closely-related Methylocystis populations, revealing differences in their history of viral interaction. Viruses infecting non-methanotrophic methylotrophs and heterotrophic predatory bacteria were also identified through the analysis of shared homologous genes, demonstrating that carbon is transferred to a diverse range of viruses associated with methane-fueled microbial food networks.

microbiology↗

Identification of a novel cobamide remodeling enzyme in the beneficial human gut bacterium Akkermansia muciniphila

The beneficial human gut bacterium Akkermansia muciniphila provides metabolites to other members of the gut microbiota by breaking down host mucin, but most of its other metabolic functions have not been investigated. A. muciniphila is known to use cobamides, the vitamin B12 family of cofactors with structural diversity in the lower ligand, though the specific cobamides it can use have not been examined. We found that growth of A. muciniphila strain MucT was nearly identical with each of seven cobamides tested, in contrast to nearly all bacteria that have been studied. Unexpectedly, this promiscuity is due to cobamide remodeling - the removal and replacement of the lower ligand - despite the absence of the canonical remodeling enzyme CbiZ in A. muciniphila. We identified a novel enzyme, CbiR, that is capable of initiating the remodeling process by hydrolyzing the phosphoribosyl bond in the nucleotide loop of cobamides. CbiR does not share homology with other cobamide remodeling enzymes or B12-binding domains, and instead is a member of the AP endonuclease 2 enzyme superfamily. We speculate that CbiR enables bacteria to repurpose cobamides they otherwise cannot use in order to grow under a cobamide-requiring condition; this function was confirmed by heterologous expression of cbiR in E. coli. Homologs of CbiR are found in over 200 microbial taxa across 22 phyla, suggesting that many bacteria may use CbiR to gain access to the diverse cobamides present in their environment. ImportanceCobamides, the vitamin B12 family of cobalt-containing cofactors, are required for metabolism in all domains of life, including most bacteria. Cobamides have structural variability in the lower ligand, and selectivity for particular cobamides has been observed in most organisms studied to date. Here, we discover that the beneficial human gut bacterium Akkermansia muciniphila can use a diverse range of cobamides due to its ability to change the cobamide structure via "cobamide remodeling". We identify and characterize the novel enzyme CbiR that is necessary for initiating the cobamide remodeling process. The discovery of this enzyme has implications not only for understanding the ecological role of A. muciniphila in the gut, but for other bacteria that carry this enzyme as well.

microbiology↗

Unexpected diversity of CPR bacteria and nanoarchaea in the rare biosphere of rhizosphere-associated grassland soil

Candidate Phyla Radiation (CPR) bacteria and nanoarchaea populate most ecosystems, but are rarely detected in soil. We concentrated particles less than 0.2 m from grassland soil, enabling targeted metagenomic analysis of these organisms, which are almost totally unexplored in soil. We recovered a diversity of CPR bacteria and some nanoarchaea sequences, but no sequences from other cellular organisms. The sampled sequences include Doudnabacteria (SM2F11) and Pacearchaeota, organisms not previously reported in soil, as well as Saccharibacteria, Parcubacteria and Microgenomates. CPR and DPANN (an acronym of the names of the first included archaea phyla) enrichments of 100-1000-fold were achieved compared to bulk soil, in which we estimate these organisms comprise about 1 to 100 cells per gram of soil. Like most CPR and DPANN sequenced to date, we predict these microorganisms live symbiotic, anaerobic lifestyles. However, Saccharibacteria, Parcubacteria, and Doudnabacteria genomes sampled here also encode ubiquinol oxidase operons that may have been acquired from other bacteria, likely during adaptation to aerobic soil environments. We posit that although present at low abundance, CPR bacteria and DPANN archaea could impact overall soil microbial community function by modulating host organism abundances and activity.

microbiology↗