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bioRxiv2021

The ecology and quantitative genetics of seed and seedling traits in upland and lowland ecotypes of a perennial grass

Plants have evolved diverse reproductive allocation strategies and seed traits to aid in dispersal, persistence in the seed bank, and establishment. In particular, seed size, dormancy, and early seedling vigor are thought to be key functional traits with important recruitment and fitness consequences across abiotic stress gradients. Selection for favored seed-trait combinations, or against maladaptive combinations, is likely an important driver shaping recruitment strategies. Here, we test for seed-trait plasticity and local adaptation in contrasting upland and lowland ecotypes of Panicum hallii with field experiments in native versus foreign habitats. Furthermore, we test whether seed traits have been under directional selection in P. hallii using the v-test (Fraser 2020) based on trait variance in a genetic cross. Finally, we evaluate the genetic architecture of ecotypic divergence for these traits with Quantitative Trait Locus (QTL) mapping. Field experiments reveal little plasticity but support a hypothesis of local adaptation among ecotypes based on recruitment. Patterns of segregation within recombinant hybrids provides strong support for directional selection driving ecotypic divergence in seeds traits. Genetic mapping revealed a polygenic architecture with evidence of genetic correlation between seed mass, dormancy, and seedling vigor. Our results suggest that the evolution of these traits may involve constraints that affect the direction of adaptive divergence. For example, seed size and germination percentage shared two colocalized QTL with antagonistic additive effects. This supports the hypothesis of a functional genetic relationship between these traits, resulting in either large seed/strong dormancy or small seed/weak dormancy trait combinations. Overall, our study provides insights into the factors facilitating and potentially constraining ecotypic differentiation in seed traits. Impact SummarySeed size and dormancy are key functional traits with important recruitment and fitness consequences. Theory suggests tradeoffs and plasticity in offspring quantity and quality are important in seed evolution. The genetics of seed size and dormancy traits have been studied extensively, but these studies are mostly limited to model system or domesticated crops. We also know very little about the genetic architecture and evolution of seed-based life history traits especially considering adaptation to xeric and mesic habitats. Here, we explored the genetic basis of trade-offs between seed size and dormancy in a C4 perennial grass, Panicum hallii, endemic to North America. We planted seeds of recombinant inbred lines from a cross between a xeric and mesic ecotype of P.hallii and mapped quantitative trait (QTL) loci for seed size, dormancy and seedling vigor traits. We detected a genetic basis of trade-offs between seed size and dormancy, suggesting that natural selection strongly favored specific trait combinations in ecotype formation. We further explored the role of seed size variation on seedling and adult recruitment in contrasting habitats. Our data showed that seed size was under strong selection through recruitment. Overall, our results demonstrate that adaptive differentiation for seed size and early life stages are important factors in adaptation to contrasting habitats.

evolutionary biology↗

bioRxiv2021

Genomic bases of insularity and ecological divergence in barn owls (Tyto alba) of the Canary Islands

Islands, and the particular organisms that populate them, have long fascinated biologists. Due to their isolation, islands offer unique opportunities to study the effect of neutral and adaptive mechanisms in determining genomic and phenotypical divergence. In the Canary Islands, an archipelago rich in endemics, the barn owl (Tyto alba) is thought to have diverged into a subspecies (T. a. gracilirostris) on the eastern islands, Fuerteventura and Lanzarote. Taking advantage of 40 whole-genomes and modern population genomics tools, we provide the first look at the origin and genetic makeup of barn owls of this archipelago. We show that the Canaries hold diverse, long-standing and monophyletic populations with a neat distinction of gene pools from the different islands. Using new method, less sensitive to structure than classical FST, to detect regions involved in local adaptation to the insular environment, we identified a haplotype-like region likely under positive selection in all Canaries individuals. Genes in this region suggest morphological adaptations to insularity. In the eastern islands, where the subspecies T. a. gracilirostris is present, genomic traces of selection pinpoint signs of locally adapted body proportions and blood pressure, consistent with the smaller size of this population living in a hot arid climate. In turn, genomic regions under selection in the western barn owls from Tenerife showed an enrichment in genes linked to hypoxia, a potential response to inhabiting a small island with a marked altitudinal gradient. Our results illustrate the interplay of neutral and adaptive forces in shaping divergence and early onset speciation.

evolutionary biology↗

bioRxiv2022

Intestinal Bacteroides Modulates Systemic Inflammation and the Microbial Ecology in a Mouse Model of CF: Evidence for Propionate and other Short Chain Fatty Acids Reducing Systemic Inflammatory Cytokines

Persons with cystic fibrosis, starting in early life, have intestinal microbiome dysbiosis characterized in part by a decreased relative abundance of the genus Bacteroides. Bacteroides is a major producer of the intestinal short chain fatty acid (SCFA) propionate. We demonstrate here that CFTR-/- Caco-2 intestinal epithelial cells are responsive to the anti-inflammatory effects of propionate. Furthermore, Bacteroides isolates inhibit the IL-1{beta}-induced inflammatory response of CFTR-/- Caco-2 intestinal epithelial cells and do so in a propionate-dependent manner. Bacteroides isolates also produce low levels of butyrate; this SCFA is positively correlated with inhibition of the inflammatory response. Finally, the introduction of Bacteroides-supplemented stool from infants with CF into the gut of CftrF508del mice results in an increase in propionate in the stool as well as the reduction in several systemic pro-inflammatory cytokines. Bacteroides supplementation also reduced the fecal relative abundance of E. coli, indicating a potential interaction between these two microbes, consistent with previous clinical studies. Together, our data indicate the important role of Bacteroides and Bacteroides-derived propionate in the context of the developing microbiome in infants and children with CF, which could help explain the observed gut-lung axis in CF.

microbiology↗

bioRxiv2022

Geographical and ecological drivers of coexistence dynamics in squamate reptiles

AO_SCPLOWBSTRACTC_SCPLOWO_ST_ABSAimC_ST_ABSSpecies richness varies widely across space. To understand the processes behind these striking patterns, we must know what are the relevant drivers underlying species coexistence. Several factors can potentially shape species coexistence such as the speciation process, the time since divergence between lineages, environmental effects, and intrinsic properties of the organisms. For the first time, we model the coexistence dynamics of lizards and snakes across broad temporal and spatial scales, investigating the role of species interactions, dispersal ability, and geographic area. LocationGlobal Time periodLast 20 million years Major taxa studiedSquamata (lizards and snakes) MethodsWe used 448 closely related species pairs and their age since divergence across 100 dated phylogenies. We categorized each pair as sympatric or allopatric and as occurring on islands or continents. We measured morphological traits to quantify niche divergence and used range and body size as proxies for dispersal ability. We applied a model-comparison framework in lizards and snakes separately to evaluate which factors best explained their coexistence dynamics. ResultsWe found that distinct factors drive the coexistence dynamics in lizards and snakes. In snakes, species pairs that coexist tend to occur on islands and are more different in body size, suggesting that both geographical setting and species interactions might be relevant factors. In contrast, we only found evidence that dispersal ability shaped the coexistence of lizards, where species coexist when they have higher dispersal abilities. Main conclusionsLizards and snakes greatly differ in coexistence dynamics. Higher heterogeneity in coexistence dynamics within lizards and group-specific life-history aspects might help to explain these findings. Our results emphasize that the interaction between where organisms are and who they are, ultimately shapes biodiversity patterns. We also highlight interesting avenues for further studies on species coexistence in deep time.

evolutionary biology↗

bioRxiv2022

Changes in interactions over ecological time scales influence single cell growth dynamics in a metabolically coupled marine microbial community

Microbial communities thrive in almost all habitats on earth. Within these communities, cells interact through the release and uptake of metabolites. These interactions can have synergistic or antagonistic effects on individual community members. The collective metabolic activity of microbial communities leads to changes in their local environment. As the environment changes over time, the nature of the interactions between cells can change. We currently lack understanding of how such dynamic feedbacks affect the growth dynamics of individual microbes and of the community as a whole. Here we study how interactions mediated by the exchange of metabolites through the environment change over time within a simple marine microbial community. We used a microfluidic-based approach that allows us to disentangle the effect cells have on their environment from how they respond to their environment. We found that the interactions between two species - a degrader of chitin and a cross-feeder that consumes metabolic by-products - changes dynamically over time as cells modify their environment. Cells initially interact positively and then start to compete at later stages of growth. Our results demonstrate that interactions between microbes are not static and depend on the state of the environment, emphasizing the importance of disentangling how modifications of the environment affects species interactions. This experimental approach can shed new light on how interspecies interactions scale up to community level processes in natural environments.

microbiology↗

bioRxiv2022

Comparing dormancy in two distantly related tunicates reveals morphological, molecular, and ecological convergences and repeated co-option

Many asexually-propagating marine invertebrates can survive extreme environmental conditions by developing dormant structures, i.e., morphologically simplified bodies that retain the capacity to completely regenerate a functional adult when conditions return to normal. Here, we examine the environmental, morphological, and molecular characteristics of dormancy in two distantly related clonal tunicate species: Polyandrocarpa zorritensis and Clavelina lepadiformis. In both species, we report that the dormant structures are able to withstand harsher temperature and salinity conditions compared to the adult, and are the dominant forms these species employ to survive the colder winter months. By finely controlling the entry and exit of dormancy in laboratory-reared individuals, we were able to select and characterize the morphology of dormant structures associated with their transcriptome dynamics. In both species, we identified putative stem and nutritive cells in structures that resemble the earliest stages of asexual propagation. By characterizing gene expression during dormancy and regeneration into the adult body plan (i.e., germination), we observed that genes which control dormancy and environmental sensing in other metazoans, notably HIF- and insulin signaling genes, are also expressed in tunicate dormancy. Germination-related genes in these two species, such as the retinoic acid pathway, are also found in other unrelated clonal tunicates during asexual development. These results are suggestive of repeated exaptation of conserved eco-physiological and regeneration programs for the origin of novel dormancy-germination processes across distantly related animal taxa.

developmental biology↗

bioRxiv2022

Ecological Observations Based on Functional Gene Sequencing Are Sensitive to the Amplicon Processing Method

Until recently, the de-facto method for short read-based amplicons reconstruction is a sequence similarity threshold approach (Operational taxonomic Units OTUs). This assumption was relaxed by shifting to Amplicon Sequencing Variants (ASVs) where distributions are fitted to abundance profiles of individual genes using a noise-error model. Whilst OTUs-based approach is still useful for 16SrRNA/18S rRNA regions, where typically 97-99% thresholds are used, their utility to functional genes is still debatable as there is no consensus on how to cluster the sequences together. Here, we compare OTUs- and ASVs-based reconstruction approaches as well as taxonomy assignment methods, Naive Bayesian Classifier (NBC) and Bayesian Lowest Common Ancestor Algorithm (BLCA), using functional genes dataset from the microbial nitrogen-cycling community in the Brouage mudflat (France). A range of OTU similarity thresholds and ASV were used to compare amoA (AOA and AOB), nxrB, nirS, nirK and nrfA communities between differing sedimentary structures. We show that for AOA-amoA and nrfA, the use of ASV led to differences in the communities between sedimentary structures whereas the use of OTUs didnt. Conversely, significant differences were detected when using OTU (97%) for AOB-amoA but not with ASV or OTUs at other similarity thresholds. Interestingly, conclusions drawn from the other three functional genes were consistent between amplicon reconstruction methods. We also show that, when the sequences in the reference-database are related to the environment in question, BLCA leads to more phylogenetically relevant classifications. However, when the reference database contains sequences more dissimilar to the ones retrieved, NBC helps obtain more information. ImportanceSeveral analysis pipelines are available to microbial ecologists to process amplicon sequencing data yet to-date, there is no consensus as to the most appropriate method, and it becomes more difficult for genes that encode a specific function (functional genes). Standardised approaches need to be adopted to increase reliability and reproducibility of environmental amplicon sequencing-based datasets. In this paper, we argue that the recently developed ASV approach offers a better opportunity to achieve such standardisation compared to OTUs for functional genes. We also propose a comprehensive framework for quality filtering of the sequencing reads based on protein sequence verification and merging.

bioinformatics↗

bioRxiv2022

Dietary Lipid Oxidization Products Alter Growth, Adiposity and Gut Microbial Ecology in Prepubertal Porcine Model

Elevated levels of dietary fats in westernized diets, associated with increased risk of obesity and other chronic diseases, are increasingly consumed by children in the United States. Cooking practices such as high heat frying and increased use of oxidizable sources of fats have introduced high levels of lipid oxidation products (LOPs) into these diets. The effects of these highly reactive dietary compounds on human biology are largely unstudied, especially in the gut where these compounds are likely present at higher concentrations. Given that the gut microbiome can be influenced by dietary components and then in turn have a systemic impact, we investigated the effects of consuming LOPs on gut bacterial and fungal communities and on growth and body composition during the prepubertal period in a porcine model. The presence of LOPs in the high fat diet reduced growth and body fat gain in the model. The gut microbiome was uniquely altered by both high fat and the presence of LOPs, with notable changes in the abundances of Turicibacterales, Spriochaetales, RF39, Lactobacillales and Erysipelotrichales. The mycobiome was dominated by Kazachstania, a porcine specific yeast, which was only minimally influenced by the dietary regimen. Application of machine learning identified dietary fat and LOPs as strong predictors of body fat. The genus Methanobrevibacter was the key microbial predictor of body fat. This study highlights the need for further studies on the biological effects of LOPs which have become ubiquitous in human, livestock and pet diets in developed countries.

physiology↗

bioRxiv2022

Climatic niche conservatism and ecological diversification in the Holarctic cold-dwelling butterfly genus Erebia

The diversification of alpine species has been modulated by their climatic niches interacting with changing climatic conditions. The relative roles of climatic niche conservatism promoting geographical speciation and of climatic niche diversification are poorly understood in diverse temperate groups. Here, we investigate the climatic niche evolution in a species rich butterfly genus, Erebia. This Holarctic cold-dwelling genus reaches the highest diversity in European mountains. We generated a nearly complete molecular phylogeny and modelled the climatic niche evolution using geo-referenced occurrence records. We reconstructed the evolution of the climatic niche and tested how the species climatic niche width changes across the occupied climate gradient and compared two main Erebia clades, the European and the Asian clade. We further explored climatic niche overlaps among species. Our analyses revealed that the evolution of Erebia has been shaped by climatic niche conservatism, supported by a strong phylogenetic signal and niche overlap in sister species, likely promoting allopatric speciation. The European and the Asian clades evolved their climatic niches toward different local optima. In addition, species in the European clade have narrower niches compared to the Asian clade. Contrasts among the clades may be related to regional climate differences, with lower climate seasonality in Europe compared to Central Asia favouring the evolution of narrower niches. Further, adaptive divergence could appear in other traits, such as habitat use, which can be reflected by narrower climatic niches detected in the European clade. In conclusion, our study extends knowledge about the complexity of evolutionary drivers in temperate insects.

evolutionary biology↗

bioRxiv2022

A reproducible and tunable synthetic soil microbial community provides new insights into microbial ecology

Microbial soil communities form commensal relationships with plants to promote the growth of both parties. Optimization of plant-microbe interactions to advance sustainable agriculture is an important field in agricultural research. However, investigation in this field is hindered by a lack of model microbial community systems and efficient approaches for building these communities. Two key challenges in developing standardized model communities are maintaining community diversity over time and storing/resuscitating these communities after cryopreservation, especially considering the different growth rates of organisms. Here, a model community of 17 soil microorganisms commonly found in the rhizosphere of diverse plant species, isolated from soil surrounding a single switchgrass plant, has been developed and optimized for use with fabricated ecosystem devices (EcoFABs). EcoFABs allow reproducible research in model plant systems, with precise control of environmental conditions and easy measurement of plant-microbe metrics. The model soil community grows reproducibly in vitro between replicates and experiments, with high community -diversity achieved through growth in low-nutrient media and adjustment of starting composition ratios for the growth of individual organisms. The community additionally grows in EcoFAB devices and regrows with a similar composition to unfrozen communities following cryopreservation with glycerol, allowing for dissemination of the model community. Our results demonstrate the generation of a stable microbial community that can be used with EcoFAB devices and shared between research groups for maximum reproducibility. ImportanceMicrobes associate with plants in distinct soil communities, to the benefit of both the soil microbes and the plant. Interactions between plants and these microbes can improve plant growth and health and are therefore a field of study in sustainable agricultural research. In this study, a model community of 17 soil bacteria has been developed to further reproducible study of plant-soil microbe interactions. Preservation of the microbial community has been optimized for dissemination to other research settings. Overall, this work will advance soil microbe research through optimization of a robust, reproducible model community.

microbiology↗

bioRxiv2022

Landscape scale ecology of Tetracladium spp. fungal root endophytes

BackgroundThe genus Tetracladium has been traditionally regarded as an Ingoldian fungus or aquatic hyphomycete - a group of phylogenetically diverse, polyphyletic fungi which grow on decaying leaves and plant litter in streams. Recent sequencing evidence has shown that Tetracladium spp. may also exist as root endophytes in terrestrial environments, and furthermore may have beneficial effects on the health and growth of their host. However, the diversity of Tetracladium spp. communities in terrestrial systems and the factors which shape their distribution are largely unknown. ResultsUsing a fungal community internal transcribed spacer amplicon dataset from 37 UK Brassica napus fields we found that soils contained diverse Tetracladium spp., most of which represent previously uncharacterised clades. The two most abundant OTUs, related to previously described aquatic T. furcatum and T. maxilliforme, were enriched in roots relative to bulk and rhizosphere soil. For both taxa, relative abundance in roots, but not rhizosphere or bulk soil was correlated with B. napus yield. The relative abundance of T. furcatum and T. maxilliforme OTUs across compartments showed very similar responses with respect to agricultural management practices and soil characteristics. The factors shaping the relative abundance of T. furcatum and T. maxilliforme OTUs in roots was assessed using linear regression and structural equation modelling. Relative abundance of Tetracladium maxilliforme and Tetracladium furcatum in roots increased with pH, concentrations of phosphorus, and increased rotation frequency of OSR. While it decreased with increased soil water content, concentrations of extractable phosphorus, chromium, and iron. ConclusionsThe genus Tetracladium as a root colonising endophyte is a diverse and wildly distributed part of the oilseed rape microbiome that positively correlates to crop yield. The main drivers of its community composition are crop management practices and soil nutrients.

microbiology↗

bioRxiv2022

Predicting environmental and ecological drivers of human population structure

Landscape, climate, and culture can all structure human populations, but few methods are designed to disentangle the importance of these many variables. We developed a machine learning method for identifying the variables which best explain migration rates, as measured by the coalescent-based program MAPS that uses shared identical by descent tracts to infer and extrapolate spatial migration across a region of interest. We applied our method to 30 human populations in eastern Africa with high density SNP array data. The remarkable diversity of ethnicities, languages, and environments in this region offers a unique opportunity to explore the variables that shape migration and genetic structure in humans. We explored more than twenty spatial variables relating to landscape, climate, and presence of tsetse flies (an important regional disease vector). The full model explained ~40% of variance in migration rate over the past 56 generations. Precipitation, minimum temperature of the coldest month, and altitude were the most important variables. Among the three groups of tsetse flies, the most important was the fusca group which is a vector for livestock trypanosomiasis. We also performed a selection scan on a subgroup of the populations who live in Ethiopia at relatively high altitudes. We did not identify well-known high-altitude genes, but we did find signatures of positive selection related to metabolism and disease. We conclude that environment has notably shaped the migration and adaptation of human populations in eastern Africa; the remaining variance in structure is likely due to cultural factors not captured in our model.

evolutionary biology↗

bioRxiv2022

Diversity and ecology of Caudoviricetes phages with genome terminal repeats in fecal metagenomes from four Dutch cohorts

The human gut harbors numerous viruses infecting the human host, microbes and other inhabitants of the gastrointestinal tract. Most of these viruses remain undiscovered, and their influence on human health is unknown. Here we characterize viral genomes in gut metagenomic data from 1,950 individuals from four population and patient cohorts. We focus on a subset of viruses that is highly abundant in the gut, remains largely uncharacterized, and allows confident complete genome identification - phages that belong to the class Caudoviricetes and possess genome terminal repeats. We detect 1,899 species-level units belonging to this subset, 19% of which do not have complete representative genomes in major public gut virome databases. These units display diverse genomic features, are predicted to infect a wide range of microbial hosts, and on average account for < 1% of metagenomic reads. Analysis of longitudinal data from 338 individuals shows that the composition of this fraction of the virome remained relatively stable over a period of 4 years. We also demonstrate that 54 species-level units are highly prevalent (detected in > 5% of individuals in a cohort). Finally, we find 34 associations between highly prevalent phages and human phenotypes, 24 of which can be explained by the relative abundance of potential hosts.

microbiology↗

bioRxiv2022

Genomic and ecologic characteristics of the airway microbial-mucosal complex

SO_SCPLOWUMMARYC_SCPLOWO_SCPCAP C_SCPCAPO_SCPLOWPARAGRAPHC_SCPLOWLung diseases due to infection and dysbiosis affect hundreds of millions of people world-wide1-4. Microbial communities at the airway mucosal barrier are conserved and highly ordered5, reflecting symbiosis and co-evolution with human host factors6. Freed of selection to digest nutrients for the host, the airway microbiome underpins cognate management of mucosal immunity and pathogen resistance. We show here the results of the first systematic culture and whole-genome sequencing of the principal airway bacterial species, identifying abundant novel organisms within the genera Streptococcus, Pauljensenia, Neisseria and Gemella. Bacterial genomes were enriched for genes encoding antimicrobial synthesis, adhesion and biofilm formation, immune modulation, iron utilisation, nitrous oxide (NO) metabolism and sphingolipid signalling. RNA-targeting CRISPR elements in some taxa suggest the potential to prevent or treat specific viral infections. Homologues of human RO60 present in Neisseria spp. provide a possible respiratory primer for autoimmunity in systemic lupus erythematosus (SLE) and Sjogren syndrome. We interpret the structure and biogeography of airway microbial communities from clinical surveys in the context of whole-genome content, identifying features of airway dysbiosis that may presage breakdown of homeostasis during acute attacks of asthma and chronic obstructive pulmonary disease (COPD). We match the gene content of isolates to human transcripts and metabolites expressed late in airway epithelial differentiation, identifying pathways that can sustain host interactions with the microbiota. Our results provide a systematic basis for decrypting interactions between commensals, pathogens, and mucosal immunity in lung diseases of global significance.

microbiology↗

bioRxiv2022

Microcosm cultures of a complex synthetic community reveal ecology and genetics of gut microbial organization

The behavior of microbial communities depends on both taxonomic composition and physical structure. Metagenomic sequencing of fecal samples has revealed the composition of human gut microbiomes, but we remain less familiar with the spatial organization of microbes between regions such as lumen and mucosa, as well as the microbial genes that regulate this organization. To discover the determinants of spatial organization in the gut, we simulate mucosal colonization over time using an in vitro culture approach incorporating mucin hydrogel microcosms with a complex yet defined community of 123 human strains for which we generated high-quality genome assemblies. Tracking strain abundance longitudinally using shotgun metagenomic measurements, we observe distinct and strain-specific spatial organization in our cultures with strains enriched on mucin microcosms versus in supernatant, reminiscent of mucosa versus lumen enrichment in vivo. Our high taxonomic resolution data enables a comprehensive search for microbial genes that underlie this spatial organization. We identify gene families positively associated with microcosm-enrichment, including several known for biofilm and adhesion functions such as efflux pumps, gene expression regulation, and membrane proteases, as well as a novel link between a coenzyme F420 hydrogenase gene family and lipo/exopolysaccharide biosynthesis. Our strain-resolved abundance measurements also demonstrate that incorporation of microcosms yields a more diverse community than liquid-only culture by allowing co-existence of closely related strains. Altogether these findings demonstrate that microcosm culture with synthetic communities can effectively simulate lumen versus mucosal regions in the gut, providing measurements of microbial organization with high taxonomic resolution to enable identification of specific bacterial genes and functions associated with spatial structure.

microbiology↗

bioRxiv2022

Glucose PTS Modulates Pyruvate Metabolism, Bacterial Fitness, and Microbial Ecology in Oral Streptococci

Spontaneous mutants with defects in the primary glucose phosphotransferase (PTS) permease (manLMNO) of Streptococcus sanguinis SK36 showed enhanced fitness at low pH. Transcriptomics and metabolomics with a manL deletion mutant (SK36/manL) revealed redirection of pyruvate to production of acetate and formate, rather than lactate. The observations were consistent with measurements of decreased lactic acid accumulation and increased excretion of pyruvate and H2O2. Genes showing increased expression in SK36/manL included those encoding carbohydrate transporters, extracellular glycosidases, intracellular polysaccharide (IPS) metabolism, arginine deiminase, and pathways for metabolism of acetoin, ethanolamine, ascorbate and formate; along with genes required for membrane biosynthesis and adhesion. Streptococcus mutans UA159 persisted much better in biofilm co-cultures with SK36/manL than with SK36, an effect that was further enhanced by culturing the biofilms anaerobically but dampened by adding arginine to the medium. We posited that the enhanced persistence of S. mutans with SK36/manL was in part due to excess excretion of pyruvate by the latter, as addition of pyruvate to S. mutans-S. sanguinis co-cultures increased the proportions of UA159 in the biofilms. Reduction of the buffer capacity or increasing the concentration of glucose benefited UA159 when co-cultured with SK36, but not with SK36/manL; likely due to the altered metabolism and enhanced acid tolerance of the mutant. When manL was deleted in S. mutans or Streptococcus gordonii, the mutants presented altered fitness characteristics. Our study demonstrated that PTS-dependent modulation of central metabolism can profoundly affect streptococcal fitness and metabolic interactions, revealing another dimension in commensal-pathogen relationships influencing dental caries development. ImportanceDental caries is underpinned by a dysbiotic microbiome and increased acid production. As beneficial bacteria that can antagonize oral pathobionts, oral streptococci such as S. sanguinis and S. gordonii can ferment many carbohydrates, despite their relative sensitivity to low pH. We characterized the molecular basis for why mutants of glucose transporter ManLMNO of S. sanguinis showed enhanced production of hydrogen peroxide and ammonia, and improved persistence under acidic conditions. Significant metabolic shift involving more than 300 genes required for carbohydrate transport, energy production, and envelope biogenesis was observed. Significantly, manL mutants engineered in three different oral streptococci displayed altered capacities for acid production and interspecies antagonism, highlighting the potential for targeting the glucose-PTS to modulate the pathogenicity of oral biofilms.

microbiology↗

bioRxiv2022

Flexible and open-source programs for quantitative image analysis in microbial ecology

Epifluorescence microscopy is an essential tool for obtaining reliable estimates of the abundance of marine microorganisms including viruses. However, computational analysis is required to gain consistent and quantitative data from digital microscopy images. Many imaging programs are proprietary and cost-prohibitive. The currently available free imaging programs are often platform specific and/or lack the flexibility to analyze microscopy images from natural samples, such as the planktonic environment, which can contain challenges such as debris and high background signals. Here we describe two MATLAB-based open-source image analysis programs that work across computer platforms and provide the tools to analyze a range of image types and cell sizes with a user-friendly interface. The Microbial Image Analysis (MiA) program aims to provide flexibility for the selection, identification, and quantification of cells that vary in size and fluorescence intensity within natural microbial communities. The Viral Image Analysis (ViA) program aims to provide an effective means for quantifying viral abundances from epifluorescence images as well as enumerating the intensity of a primary and secondary stain. In this paper, we provide an overview of the functionality of the MiA and ViA programs and highlight specific program features through several microbial image case studies.

microbiology↗

bioRxiv2022

The TaxUMAP atlas: efficient display of large clinical microbiome data reveals ecological competition involved in protection against bacteremia

The microbiome is associated with health and disease, but causal effects are hard to quantify-- especially in humans where controlled experiments are nearly impossible. Akin to natural experiments, closely monitored patients offer an alternative to characterize microbiome effects. We present TaxUMAP, a taxonomically-informed visualization method to effectively display diverse microbiome states. TaxUMAP charts a microbiome atlas from 1,870 cancer patients as they progress through therapy-induced perturbations, and quantifies the microbiome contribution to patients risk for life-threatening bacteremia. We find that the lowest diversity states (gut dominations) that follow antibiotic treatments are stable, and that diverse communities harbor more diverse antimicrobial resistance genes than dominations. We reveal that certain Klebsiella species are associated with reduced risk for bacteremia, an effect driven by bacterial competition that we validate experimentally in vitro and in vivo. TaxUMAP effectively maps longitudinal microbiome data that can facilitate research into causal microbiome effects on human health. HIGHLIGHTSO_LITaxUMAP charts an atlas of patients microbiome states and their clinical context to reveal new causal effects. C_LIO_LIAntibiotics deplete the biodiversity and reduce the number of different antimicrobial resistance genes in the gut microbiome. C_LIO_LICertain Klebsiella species are associated with lower risk of bacteremia by other gut-borne pathogens. C_LIO_LIThese Klebsiella outcompete other gram-negative pathogens in vivo. C_LI

microbiology↗

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