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Viver, T.

Publications and source records attributed to Viver, T..

6 recordsLinked to original sources

Metagenomics reveal allopatric speciation and higher connectivity among coastal vs. inland hypersaline lakes and solar salterns

Hypersaline environments, due to their discrete and geographically isolated nature, constitute ideal systems for studying evolutionary patterns and microbial diversification, and especially here when contrasting coastal with inland systems. Based on metagenomic comparisons of 25 hypersaline sites across 11 countries, we explored the influence of environmental factors, ionic composition, and geographic distance on their microbial community structures and taxa diversification. Our results revealed that microbial communities from coastal environments were taxonomically and functionally more similar to each other than to those from inland sites. A distance-decay relationship in the genetic relatedness, significantly more pronounced for the coastal sites, was observed among reconstructed metagenome-assembled genomes (MAGs), clearer at distances below 400 km, but still detectable across global scales up to 20,000 km. The 484 MAGs recovered, representing 284 distinct species, revealed a striking global ubiquity, with 62.5% of the species showed cosmopolitanism as were detected across multiple sites. The higher taxonomic and genetic similarity of coastal environments over the inland sites seems to reflect an environmental connection that may be related to the ocean current dynamics. Most cosmopolitan species showed clear allopatric differentiation, although few cases of a single globally dominant genomovar (average nucleotide identity, ANI > 99.8%) were also observed, especially for some Haloquadratum species. The findings suggest that coastal hypersaline systems are loosely constrained by geographic isolation, with clear signals of allopatric speciation at the mesoscale (tenths to hundreds of kilometers) that become blurrier at larger scales.

microbiology↗

Deep long-read metagenomic sequencing reveals niche differentiation in carbon cycling potential between benthic and planktonic microbial populations

Coastal marine sediments function as large-scale natural biocatalytic filters, remineralizing and transforming organic matter. Benthic microbiomes exhibit remarkable temporal stability, contrasting with the dynamic, substrate-driven successions of bacterioplankton. Nonetheless, understanding their role in carbon cycling and interactions between these microbial groups is limited due to the complexity of benthic microbiomes. Here, we used a seasonally resolved, deep short- and long-read metagenomic approach to examine distinctive genomic features of microbiomes recovered from sediment, the overlaying water column, and particle-attached bacteria and archaea in the North Sea. We recovered 115 benthic metagenome-assembled genomes (MAGs) that belonged to Woeseiales, Rhizobiales, Planctomycetia, Gemmatimonadota, and Desulfobacterota species. While Proteobacteria and Actinobacteriota were characteristic phyla of sediments, Acidimicrobiia and Desulfocapsaceae species were shared between sediments and particle-attached fractions of the water column, indicative of significant bentho-pelagic coupling. Predominant members of the family Woeseiaceae carried polysaccharide utilization loci (PULs) predicted to target laminarin, alginate, and -glucan in sediments. In contrast, water column species lacked PULs and encoded a significantly higher fraction of sulfatases and peptidases, indicating a role in the degradation of protein-rich and sulfated organic matter. Our findings disentangle family-level adaptations and niche differentiation between globally significant benthic and water column populations involved in marine organic matter degradation and carbon storage.

microbiology↗

Microbial species exist and are maintained by ecological cohesiveness coupled to high homologous recombination.

Recent analyses of metagenomes and genomes have revealed that microbial communities are predominantly composed of persistent, sequence-discrete species and intraspecies units (genomovars). To advance the species concept the underlying genetic or ecological mechanisms that maintain these discrete units need to be elucidated. By analyzing closely related isolate genomes from the same or related samples we show that high ecological cohesiveness coupled to frequent-enough and unbiased (i.e., not selection driven) horizontal gene flow, mediated by homologous recombination, often underlie these diversity patterns. Ecological cohesiveness was inferred based on higher similarity in abundance patterns of genomes of the same vs. different units, while recombination frequency was shown to have two times or more impact on sequence evolution than point mutation. Therefore, our results represent a departure compared to previous models of microbial speciation that invoke either ecology or selection-driven recombination, but not their synergistic effect, as the mechanism of unit cohesion. These results were observed in both Salinibacter ruber, an environmental halophilic organism, and Escherichia coli, the model gut-associated organism and an opportunistic pathogen, indicating that they may be more broadly applicable to the microbial world. Therefore, our results have strong implications for how to identify and regulate microbial species and genomovars of clinical or environmental importance and answer an important question for microbiology: what a species is. SIGNIFICANCEA highly pressing issue to resolve toward advancing the species concept for microbes (i.e., "what a species is") is to elucidate the underlying mechanisms for creating and maintaining species- and intraspecies-level gaps in diversity, or simply "clusters". In this study, we provide a novel methodology and the appropriate data to elucidate these mechanisms, and thus provide a mechanistic explanation of how the evolution of species- and strain-level clusters takes place. Specifically, our results show that several bacteria may be evolving and speciating much more sexually than previously thought, even under conditions of no strong positive selection for DNA exchange (i.e., neutral conditions). These results have major implications for better understanding and modeling microbial diversity on the planet.

microbiology↗

Towards estimating the number of strains that make up a natural bacterial population

What a strain is and how many strains make up a natural bacterial population remain elusive concepts despite their apparent importance for assessing the role of intra-population diversity in disease emergence or response to environmental perturbations. To advance these concepts, we sequenced 138 randomly selected Salinibacter ruber isolates from two solar salterns and assessed these genomes against companion short-read metagenomes from the same samples. The distribution of genome-aggregate average nucleotide identity (ANI) values among these isolates revealed a bimodal distribution, with significantly lower occurrence of values between 99.2% and 99.8% relative to ANI >99.8% or <99.2%, revealing a natural "gap" in the sequence space within species. Accordingly, we used this ANI gap to define genomovars and a higher ANI value of >99.99% and shared gene-content >99.0% to define strains. Using these thresholds and extrapolating from how many metagenomic reads each genomovar uniquely recruited, we estimated that -although our 138 isolates represented about 80% of the Sal. ruber population- the total population in one pond is composed of 5,500 to 11,000 genomovars, the great majority of which appear to be rare in situ. These data also revealed that the most frequently recovered isolate in lab media was often not the most abundant genomovar in situ, suggesting that cultivation biases are significant, even in cases that cultivation procedures are thought to be robust. Preliminary analyses of available genomes revealed that the thresholds used for defining strains and distinct intra-species units (genomovars) may be broadly applicable to additional bacterial species. Significance StatementStrains are the smallest distinguishable units within a microbial species. Strains that carry unique gene content often underly the emergence of disease outbreaks and the response of the species to environmental perturbations. Therefore, a major challenge in microbiome research across environmental and clinical settings is to evaluate how many strains of the same species coexist in nature and how dominant strains emerge from this diversity. Unfortunately, the available theoretical concept of strain is not directly applicable to culture-independent surveys. Here, we provide such a practical definition for strain and use it to show that that the number of strains making up a natural bacterial population may be large, in the order of a few thousands, but not infinite.

microbiology↗

A natural definition for a bacterial strain and clonal complex

Large-scale surveys of prokaryotic communities (metagenomes) as well as isolate genomes have revealed that their diversity is predominantly organized in sequence-discrete units that may be equated to species. Specifically, genomes of the same species commonly show genome-aggregate average nucleotide identity (ANI) >95% among themselves and ANI <90% to members of other species, while genomes showing ANI 90-95% are comparatively rare. However, it remains unclear if such "discontinuities" or gaps in ANI values can be observed within species and thus, used to advance and standardize intra-species units such as strains and sequence types. By analyzing 18,123 complete isolate genomes from 330 bacterial species with at least ten genome representatives each as well as available long-read metagenomes, we show that such a discontinuity exists between 99.2-99.8% (mean 99.5%) ANI. The 99.5% ANI threshold is largely consistent with how sequence types have been defined in previous epidemiological studies but provides clusters with [~]20% higher accuracy in terms of evolutionary and gene-content relatedness of the grouped genomes, while strains should be consequently defined at higher ANI values (>99.99% proposed). Collectively, our results should facilitate future micro-diversity studies across clinical or environmental settings because they provide a more natural definition of intra-species units of diversity.

microbiology↗

Toward quantifying the adaptive role of bacterial pangenomes during environmental perturbations

Metagenomic surveys have revealed that natural microbial communities are predominantly composed of sequence-discrete, species-like populations but the genetic and/or ecological mechanisms that maintain such populations remain speculative, limiting our understanding of population speciation and adaptation to environmental perturbations. To address this knowledge gap, we sequenced 112 Salinibacter ruber isolates and 12 companion metagenomes recovered from four adjacent saltern ponds in Mallorca, Spain that were experimentally manipulated to dramatically alter salinity and light intensity, the two major drivers of these ecosystems. Our analyses showed that the pangenome of the local Sal. ruber population is open and similar in size ([~]15,000 genes) to that of randomly sampled Escherichia coli genomes. While most of the accessory (non-core) genes showed low in situ coverage based on the metagenomes compared to the core genes, indicating that they were functionally unimportant and/or ephemeral, 3.49% of them became abundant when salinity (but not light intensity) conditions changed and encoded for functions related to osmoregulation. Nonetheless, the ecological advantage of these genes, while significant, was apparently not strong enough to purge diversity within the population. Collectively, our results revealed a possible mechanism for how this immense gene diversity is maintained, which has implications for the prokaryotic species concept. Significance StatementThe pangenomes of bacterial species, i.e., the number of non-redundant genes carried by members of the species, can be enormous based on the genome sequencing of isolates from various sites around the globe and different years. However, to what extent this pattern of gene diversity applies to natural bacterial populations, i.e., strains co-occurring in the same site, and the value of this diversity for population adaptation during environmental transition remains unclear. This study showed that while the pangenome of a natural population can be similarly large, only a small fraction of the pangenome appears to be functionally important when conditions change. Taken together, these results provided quantitative insights into the extent and functional significance of the accessory pangenome of a natural, species-like population.

microbiology↗