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ISME Communications, Volume 1, pp 1-10; https://doi.org/10.1038/s43705-021-00044-w
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ISME Communications, Volume 1, pp 1-4; https://doi.org/10.1038/s43705-021-00060-w
Lichen thalli are formed through the symbiotic association of a filamentous fungus and photosynthetic green alga and/or cyanobacterium. Recent studies have revealed lichens also host highly diverse communities of secondary fungal and bacterial symbionts, yet few studies have examined the viral component within these complex symbioses. Here, we describe viral biodiversity and functions in cyanolichens collected from across North America and Europe. As current machine-learning viral-detection tools are not trained on complex eukaryotic metagenomes, we first developed efficient methods to remove eukaryotic reads prior to viral detection and a custom pipeline to validate viral contigs predicted with three machine-learning methods. Our resulting high-quality viral data illustrate that every cyanolichen thallus contains diverse viruses that are distinct from viruses in other terrestrial ecosystems. In addition to cyanobacteria, predicted viral hosts include other lichen-associated bacterial lineages and algae, although a large fraction of viral contigs had no host prediction. Functional annotation of cyanolichen viral sequences predicts numerous viral-encoded auxiliary metabolic genes (AMGs) involved in amino acid, nucleotide, and carbohydrate metabolism, including AMGs for secondary metabolism (antibiotics and antimicrobials) and fatty acid biosynthesis. Overall, the diversity of cyanolichen AMGs suggests that viruses may alter microbial interactions within these complex symbiotic assemblages.
ISME Communications, Volume 1, pp 1-9; https://doi.org/10.1038/s43705-021-00058-4
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ISME Communications, Volume 1, pp 1-5; https://doi.org/10.1038/s43705-021-00057-5
Conjugative plasmids bestow important traits to microbial communities, such as virulence, antibiotic resistance, pollutant biotransformation, and biotechnology-relevant functions. While the biological mechanisms and determinants of plasmid conjugation are well established, the underlying physical and ecological driving forces remain unclear. Microbial communities often inhabit unsaturated environments, such as soils and host surfaces (e.g., skin, teeth, leaves, roots), where water evaporation and associated small-scale hydrodynamic processes frequently occur at numerous air-water and solid-water interfaces. Here, we hypothesized that evaporation can induce water flows with profound effects on the spatial distribution and surface deposition of cells, and consequently on the extent of plasmid conjugation. Using droplet experiments with an antibiotic resistance-encoding plasmid, we show that evaporation-induced water flows reduce cell-cell distances and significantly increase the extent of plasmid conjugation. Counterintuitively, we found that evaporation results in lower expression levels of conjugation-related genes. This negative relationship between the extent of plasmid conjugation and the expression of conjugation-related genes could be attributed to increased conjugation efficiency during evaporation. This study provides new insights into the physical and ecological determinants of plasmid conjugation, with important implications for understanding the spread and proliferation of plasmid-encoded traits.
ISME Communications, Volume 1, pp 1-9; https://doi.org/10.1038/s43705-021-00056-6
Earth’s aquatic food webs are overwhelmingly supported by planktonic microalgae that live in the sunlit water column where only a minimum number of physical niches are readily identifiable. Despite this paucity of environmental differentiation, these “phytoplankton” populations exhibit a rich biodiversity, an observation not easily reconciled with broadly accepted rules of resource-based competitive exclusion. This conundrum is referred to as the “Paradox of the Plankton”. Consideration of physical distancing between nutrient depletion zones around individual phytoplankton, however, suggests a competition-neutral resource landscape. Application of neutral theory to the sheer number of phytoplankton in physically-mixed water masses yields a prediction of astronomical biodiversity, suggesting the inverted paradox: Why are there so few phytoplankton species? Here, we introduce a trophic constraint on phytoplankton that, when combined with stochastic principals of ecological drift, predicts only modest levels of diversity in an otherwise competition-neutral landscape. Our “trophic exclusion” principle predicts diversity to be independent of population size and yields a species richness across cell-size classes that is consistent with broad oceanographic survey observations.
ISME Communications, Volume 1, pp 1-10; https://doi.org/10.1038/s43705-021-00052-w
Winogradskyella is a genus within the phylum Bacteroidetes with a clear marine origin. Most members of this genus have been found associated with marine animals and algae, but also with inorganic surfaces such as sand. In this study, we analyzed genomes of eleven species recently isolated from surface seawater samples from the North Sea during a single spring algae bloom. Corresponding metagenomes yielded a single Candidatus species for this genus. All species in culture, with the exception of W. ursingii, affiliated with a Winogradskyella lineage characterized by large genomes (~4.3 ± 0.4 Mb), with high complexity in their carbohydrate and protein degradation genes. Specifically, the polysaccharide utilization loci (PULs) were diverse within each individual strain, indicating large substrate versatility. Although present in the North Sea, the abundances of these strains were at, or below, the detection limit of the metagenomes. In contrast, the single species, classified as Candidatus W. atlantica, to which all North Sea MAGs belonged, affiliated with a lineage in which the cultivated representatives showed small genomes of ~3.0–3.5 Mb, with the MAGs having ~2.3 Mb. In Ca. W. atlantica, genome streamlining has apparently resulted in the loss of biosynthesis pathways for several amino acids including arginine, methionine, leucine and valine, and the PUL loci were reduced to a single one for utilizing laminarin. This as-yet uncultivated species seems to capitalize on sporadically abundant substrates that are released by algae blooms, mainly laminarin. We also suggest that this streamlined genome might be responsible for the lack of growth on plates for this Candidatus species, in contrast to growth of the less abundant but coexisting members of the genus.
ISME Communications, Volume 1, pp 1-10; https://doi.org/10.1038/s43705-021-00055-7
The functioning of microbial ecosystems has important consequences from global climate to human health, but quantitative mechanistic understanding remains elusive. The components of microbial ecosystems can now be observed at high resolution, but interactions still have to be inferred e.g., a time-series may show a bloom of bacteria X followed by virus Y suggesting they interact. Existing inference approaches are mostly empirical, like correlation networks, which are not mechanistically constrained and do not provide quantitative mass fluxes, and thus have limited utility. We developed an inference method, where a mechanistic model with hundreds of species and thousands of parameters is calibrated to time series data. The large scale, nonlinearity and feedbacks pose a challenging optimization problem, which is overcome using a novel procedure that mimics natural speciation or diversification e.g., stepwise increase of bacteria species. The method allows for curation using species-level information from e.g., physiological experiments or genome sequences. The product is a mass-balancing, mechanistically-constrained, quantitative representation of the ecosystem. We apply the method to characterize phytoplankton—heterotrophic bacteria interactions via dissolved organic matter in a marine system. The resulting model predicts quantitative fluxes for each interaction and time point (e.g., 0.16 µmolC/L/d of chrysolaminarin to Polaribacter on April 16, 2009). At the system level, the flux network shows a strong correlation between the abundance of bacteria species and their carbon flux during blooms, with copiotrophs being relatively more important than oligotrophs. However, oligotrophs, like SAR11, are unexpectedly high carbon processors for weeks into blooms, due to their higher biomass. The fraction of exudates (vs. grazing/death products) in the DOM pool decreases during blooms, and they are preferentially consumed by oligotrophs. In addition, functional similarity of phytoplankton i.e., what they produce, decouples their association with heterotrophs. The methodology is applicable to other microbial ecosystems, like human microbiome or wastewater treatment plants.
ISME Communications, Volume 1, pp 1-14; https://doi.org/10.1038/s43705-021-00053-9
The domestication of the laboratory mouse has influenced the composition of its native gut microbiome, which is now known to differ from that of its wild ancestor. However, limited exploration of the rodent gut microbiome beyond the model species Mus musculus has made it difficult to interpret microbiome variation in a broader phylogenetic context. Here, we analyse 120 de novo and 469 public metagenomically-sequenced faecal and caecal samples from 16 rodent hosts representing wild, laboratory and captive lifestyles. Distinct gut bacterial communities were observed between rodent host genera, with broadly distributed species originating from the as-yet-uncultured bacterial genera UBA9475 and UBA2821 in the families Oscillospiraceae and Lachnospiraceae, respectively. In laboratory mice, Helicobacteraceae were generally depleted relative to wild mice and specific Muribaculaceae populations were enriched in different laboratory facilities, suggesting facility-specific outgrowths of this historically dominant rodent gut family. Several bacterial families of clinical interest, including Akkermansiaceae, Streptococcaceae and Enterobacteriaceae, were inferred to have gained over half of their representative species in mice within the laboratory environment, being undetected in most wild rodents and suggesting an association between laboratory domestication and pathobiont emergence.
ISME Communications, Volume 1, pp 1-4; https://doi.org/10.1038/s43705-021-00051-x
Land use change has long-term effects on the structure of soil microbial communities, but the specific community assembly processes underlying these effects have not been identified. To investigate effects of historical land use on microbial community assembly, we sampled soils from several currently forested watersheds representing different historical land management regimes (e.g., undisturbed reference, logged, converted to agriculture). We characterized bacterial and fungal communities using amplicon sequencing and used a null model approach to quantify the relative importance of selection, dispersal, and drift processes on bacterial and fungal community assembly. We found that bacterial communities were structured by both selection and neutral (i.e., dispersal and drift) processes, while fungal communities were structured primarily by neutral processes. For both bacterial and fungal communities, selection was more important in historically disturbed soils compared with adjacent undisturbed sites, while dispersal processes were more important in undisturbed soils. Variation partitioning identified the drivers of selection to be changes in vegetation communities and soil properties (i.e., soil N availability) that occur following forest disturbance. Overall, this study casts new light on the effects of historical land use on soil microbial communities by identifying specific environmental factors that drive changes in community assembly.
ISME Communications, Volume 1, pp 1-11; https://doi.org/10.1038/s43705-021-00050-y
Other than the Methanobacteriales and Methanomassiliicoccales, the characteristics of archaea that inhabit the animal microbiome are largely unknown. Methanimicrococcus blatticola, a member of the Methanosarcinales, currently reunites two unique features within this order: it is a colonizer of the animal digestive tract and can only reduce methyl compounds with H2 for methanogenesis, a increasingly recognized metabolism in the archaea and whose origin remains debated. To understand the origin of these characteristics, we have carried out a large-scale comparative genomic analysis. We infer the loss of more than a thousand genes in M. blatticola, by far the largest genome reduction across all Methanosarcinales. These include numerous elements for sensing the environment and adapting to more stable gut conditions, as well as a significant remodeling of the cell surface components likely involved in host and gut microbiota interactions. Several of these modifications parallel those previously observed in phylogenetically distant archaea and bacteria from the animal microbiome, suggesting large-scale convergent mechanisms of adaptation to the gut. Strikingly, M. blatticola has lost almost all genes coding for the H4MPT methyl branch of the Wood–Ljungdahl pathway (to the exception of mer), a phenomenon never reported before in any member of Class I or Class II methanogens. The loss of this pathway illustrates one of the evolutionary processes that may have led to the emergence of methyl-reducing hydrogenotrophic methanogens, possibly linked to the colonization of organic-rich environments (including the animal gut) where both methyl compounds and hydrogen are abundant.