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bioRxiv2022

"Same same but different"Exploring evolutionary and ecological causes of eye diversification in bumblebees

Bees rely heavily on vision during most of their interaction with the environment, but so far, visual abilities have not been included into functional investigations of these crucial pollinators. This is probably due to the lack of comprehensive and phylogenetically-controlled quantification of visual traits across species. In the present study, we used high-throughput micro-CT tools to quantify, compare and understand the diversity of visual traits of compound eyes in bumblebees. Visual systems of bumblebees were far from identical, with variations across sizes, castes and species. While phylogenetic proximity poorly supported interspecific variations, these were better explained by two ecological factors: social parasitism and habitat. The eye parameter - a metric that measures the relative investment of a compound eye into resolution or sensitivity - was lower in queens of social parasitic species than of non-parasitic species. Workers of species associated with forested habitat had distinct visual traits, including a higher eye parameter, than those of species living in open landscapes. These diverse visual traits are likely to provide selective advantages to bumblebees given their specific ecological requirements. We thus propose that social parasitism and forest habitat are drivers of the diversification of compound eyes in bumblebees. Finally, we discuss how the present study can inspire trait-based approaches in ecology and conservation biology.

neuroscience↗

bioRxiv2022

Diversity and ecological function of urease-producing bacteria in the cultivation environment of Gracilariopsis lemaneiformis

Urease-producing bacteria (UPB) provide inorganic nitrogen for primary producers by hydrolysis of urea. They play an important role in marine nitrogen cycle. However, there is still incomplete understanding of UPB and their ecological functions in the cultivation environment of red macroalage Gracilariopsis lemaneiformis. This study comprehensively analyzed the diversity of culturable UPB and explored their effects on urea uptake by G. lemaneiformis. Total 34 isolates belonging to four main bacterial phyla i.e. Proteobacteria, Bacteroidetes, Firmicutes, and Actinobacteria were identified through 16S rRNA sequencing and were screened for UPB by urea agar chromogenic medium assay and ureC gene cloning. Our data revealed that only 8 strains were found containing urease. These all UPB exhibited different urease activities by Berthelot reaction colorimetry assay. Furthermore, UPB with highest urease activity was selected to use as co-culture with G. lemaneiformis to explore its role in terms of promotion or inhibition of nitrogen uptake by G. lemaneiformis. The results showed that the urea consumption in culture media and the total cellular nitrogen in G. lemaneiformis found increased significantly in the UPB-co culture group than control i.e. in the sterile group (p < 0.05). Similarity, isotopic assay revealed that {delta}15N contents of G. lemaneiformis was significant higher in the UPB-co culture than in the control where {delta}15N-urea was the only nitrogen source in the culture media, indicating the UPB helped G. lemaneiformis to absorb more nitrogen from urea. Moreover, the highest content of {delta}15N was found in G. lemaneiformis with epiphytic bacteria, as compared to sterilized (control) showing that epiphytic bacteria along with UPB have compound effects in helping G. lemaneiformis absorb more nitrogen in urea. Taken together, these results provide unique insight into the ecological role of UPB and suggest that urease from macroalgae environment-associated bacteria might be important player in the marine nitrogen cycling. ImportanceTo the best of our knowledge, this is the first study ever conducted to isolate the culturable UPB from the cultivation environment of G. lemaneiformis by urea agar chromogenic medium assay, and also evaluate the effects of UPB on urea utilization in G. lemaneiformis by stable isotopic tracer technique. This study provides a new insight into the mechanism of organic nitrogen uptake and utilization in G. lemaneiformis, and is of great significance for a better understanding of the ecological role of functional bacteria (e.g. urease-producing bacteria) in the marine nitrogen cycling.

microbiology↗

bioRxiv2023

Comparative phylogeography reveals widespread cryptic diversity driven by ecology in Panamanian birds

Widespread species often harbor unrecognized genetic diversity, and investigating the factors associated with such cryptic variation can help us better understand the forces driving diversification. Here, we identify potential cryptic species based on a comprehensive dataset of COI mitochondrial DNA barcodes from 2,333 individual Panamanian birds across 429 species, representing 391 (59%) of the 659 resident landbird species of the country, as well as opportunistically sampled waterbirds. We complement this dataset with additional publicly available mitochondrial loci, such as ND2 and cytochrome b, obtained from whole mitochondrial genomes from 20 taxa. Using barcode identification numbers (BINs), we find putative cryptic species in 19% of landbird species, highlighting hidden diversity in the relatively well-described avifauna of Panama. Whereas some of these mitochondrial divergence events corresponded with recognized geographic features that likely isolated populations, such as the Cordillera Central highlands, the majority (74%) of lowland splits were between eastern and western populations. The timing of these splits are not temporally coincident across taxa, suggesting that historical events, such as the formation of the Isthmus of Panama and Pleistocene climatic cycles, were not the primary drivers of cryptic diversification. Rather, we observed that forest species, understory species, insectivores, and strongly territorial species--all traits associated with lower dispersal ability--were all more likely to have multiple BINs in Panama, suggesting strong ecological associations with cryptic divergence. Additionally, hand-wing index, a proxy for dispersal capability, was significantly lower in species with multiple BINs, indicating that dispersal ability plays an important role in generating diversity in Neotropical birds. Together, these results underscore the need for evolutionary studies of tropical bird communities to consider ecological factors along with geographic explanations, and that even in areas with well-known avifauna, avian diversity may be substantially underestimated. LAY SUMMARY- What factors are common among bird species with cryptic diversity in Panama? What role do geography, ecology, phylogeographic history, and other factors play in generating bird diversity? - 19% of widely-sampled bird species form two or more distinct DNA barcode clades, suggesting widespread unrecognized diversity. - Traits associated with reduced dispersal ability, such as use of forest understory, high territoriality, low hand-wing index, and insectivory, were more common in taxa with cryptic diversity. Filogeografia comparada revela amplia diversidad criptica causada por la ecologia en las aves de Panama RESUMENEspecies extendidas frecuentemente tiene diversidad genetica no reconocida, y investigando los factores asociados con esta variacion criptica puede ayudarnos a entender las fuerzas que impulsan la diversificacion. Aqui, identificamos especies cripticas potenciales basadas en un conjunto de datos de codigos de barras de ADN mitocondrial de 2,333 individuos de aves de Panama en 429 especies, representando 391 (59%) de las 659 especies de aves terrestres residentes del pais, ademas de algunas aves acuaticas muestreada de manera oportunista. Adicionalmente, complementamos estos datos con secuencias mitocondriales disponibles publicamente de otros loci, tal como ND2 o citocroma b, obtenidos de los genomas mitocondriales completos de 20 taxones. Utilizando los numeros de identificacion de codigo de barras (en ingles: BINs), un sistema taxonomico numerico que proporcina una estimacion imparcial de la diversidad potencial a nivel de especie, encontramos especies cripticas putativas en 19% de las especies de aves terrestres, lo que destaca la diversidad oculta en la avifauna bien descrita de Panama. Aunque algunos de estos eventos de divergencia conciden con caracteristicas geograficas que probablemente aislaron las poblaciones, la mayoria (74%) de la divergencia en las tierras bajas se encuentra entre las poblaciones orientales y occidentales. El tiempo de esta divergencia no coincidio entre los taxones, sugiriendo que eventos historicos tales como la formacion del Istmo de Panama y los ciclos climaticos del pleistoceno, no fueron los principales impulsores de la especiacion. En cambio, observamos asociaciones fuertes entre las caracteristicas ecologicas y la divergencia mitocondriale: las especies del bosque, sotobosque, con una dieta insectivora, y con territorialidad fuerte mostraton multiple BINs probables. Adicionalmente, el indice mano-ala, que esta asociado a la capacidad de dispersion, fue significativamente menor en las especies con BINs multiples, sugiriendo que la capacidad de dispersion tiene un rol importamente en la generacion de la diversidad de las aves neotropicales. Estos resultos demonstran la necesidad de que estudios evolutivos de las comunidades de aves tropicales consideren los factores ecologicos en conjunto con las explicaciones geograficos. Palabras clave: biodiversidad tropical, biogeografia, codigos de barras, dispersion, especies cripticas

evolutionary biology↗

bioRxiv2023

Climatic niches provide insights into the evolutionary origins and ecological significance of the succulent CAM syndrome around the world

Although distributed globally, plants possessing the succulent syndrome are thought to have evolved to adapt to arid climates, because they possess modifications that increase their water use efficiency. Here we study the evolution and the ecological nature of the succulent CAM syndrome at a global scale by analyzing the climatic niches of succulents within the Caryophyllales, testing the hypothesis of a climatic niche specialization by comparing them with their non-succulent, non-arid adapted relatives. We assembled and carefully curated a worldwide dataset of 5447 species in 28 families, and analyzed the current and evolutionary trajectories of climatic niches with an array of statistical methods including ecological niche modeling, phylogenetic regression and divergence dates estimation. Our results confirm the Core Caryophyllales tend to inhabit drylands probably since their origin in the Early Cretaceous. However, the succulent syndrome appeared later with some lineages diversifying profusely afterwards. The climatic niche of succulents is not differentiated from their non-succulent relatives, but narrower, and contained within the non-succulents, showing no relationship with extreme conditions such as high aridity or temperatures. Our results support alternative interpretations of the origin of the CAM syndrome and the ecological significance of succulence, as well as the prolific radiation of richest lineages. HighlightsThe climatic niche occupied by succulent CAM plants is not different from their non-succulent relatives. Estimated dates and character reconstruction suggest CO2 scarcity as the evolutionary pressure under these plants originated.

plant biology↗

bioRxiv2023

Multiple axes of visual system diversity in Ithomiini, an ecologically diverse tribe of mimetic butterflies

The striking structural variation seen in arthropod visual systems can be explained by the overall quantity and spatio-temporal structure of light within habitats coupled with developmental and physiological constraints. However, little is currently known about how fine-scale variation in visual structures arise across shorter evolutionary and ecological scales. In this study, we characterise patterns of interspecific (between species), intraspecific (between sexes) and intraindividual (between eye regions) variation in the visual system of four ithomiine butterfly species. These species are part of a diverse 26-Myr-old Neotropical radiation where changes in mimetic colouration are associated with fine-scale shifts in ecology, such as microhabitat preference. By using a combination of selection analyses on visual opsin sequences, in-vivo ophthalmoscopy, micro-computed tomography (micro-CT), immunohistochemistry, confocal microscopy, and neural tracing, we quantify and describe physiological, anatomical, and molecular traits involved in visual processing. Using these data, we provide evidence of substantial variation within the visual systems of Ithomiini, including: i) relaxed selection on visual opsins, perhaps mediated by habitat preference, ii) interspecific shifts in visual system physiology and anatomy, and iii) extensive sexual dimorphism, including the complete absence of a butterfly-specific optic neuropil in the males of some species. We conclude that considerable visual system variation can exist within diverse insect radiations, hinting at the evolutionary lability of these systems to rapidly develop specialisations to distinct visual ecologies, with selection acting at both the perceptual, processing, and molecular level. Summary statementPhysiological, anatomical, and molecular evidence of extensive visual system variation within a diverse butterfly radiation, hinting at the lability of visual systems to evolve specialisations to distinct visual environments.

evolutionary biology↗

bioRxiv2023

Capturing dynamic fear experiences in naturalistic contexts: An ecologically valid fMRI signature integrating brain activation and connectivity

Enhancing our understanding of how the brain constructs conscious emotional experiences within dynamic real-life contexts necessitates ecologically valid neural models. Here, we present evidence delineating the constraints of current fMRI activation models in capturing naturalistic fear dynamics. To address this challenge, we fuse naturalistic fMRI with predictive modeling techniques to develop an ecologically valid fear signature that integrates activation and connectivity profiles, allowing for accurate prediction of subjective fear experience under highly dynamic close-to-real-life conditions. This signature arises from insights into the crucial role of distributed brain networks and their interactions in emotion modulation, and the potential of network-level information to improve predictions in dynamic contexts. Across a series of investigations, we demonstrate that this signature predicts stable and dynamic fear experiences across naturalistic scenarios with heightened sensitivity and specificity, surpassing traditional activation- and connectivity-based signatures. Notably, the integration of affective connectivity profiles enables accurate real-time predictions of fear fluctuations in naturalistic settings. Additionally, we unearth a distributed yet redundant brain-wide representation of fear experiences. Subjective fear is encoded not only by distributed cortical and subcortical regions but also by their interactions, with no single brain system conveying substantial unique information. Our study establishes a comprehensive and ecologically valid functional brain architecture for subjective fear in dynamic environments and bridges the gap between experimental neuroscience and real-life emotional experience.

neuroscience↗

bioRxiv2023

From populations to pan-genomes: investigating the role of ecology and genomic architecture in maintaining species boundaries in the porcini mushroom, Boletus edulis

Hybridization among diverged species is common across all domains of eukaryotic life, but appears to be particularly common in fungi. However, some fungi exhibit a greater tendency for hybridization than others and it is unclear what mechanisms facilitate or prevent hybridization. Here, we generated 253 whole genome sequences and 22 reference genomes within the globally distributed ectomycorrhizal species complex Boletus edulis Bull. and use a multi-faceted genomic approach to identify patterns of ongoing hybridization and determine whether hybridization is mediated by changes in genome structure, ecology, or both. We found that hybridization is common among species of B. edulis despite 2.1 million years of divergence. However, not all lineages that hybridize today exhibit patterns of introgression, indicating the presence of strong reproductive boundaries among some species. Using a pan-genomic approach we find that genome structural variation is abundant within B. edulis, but that the presence of ongoing introgression does not correlate with genome structural similarity or overall gene content. Instead, we find that the composition of ecologically relevant gene families more accurately predicts the presence of introgression among lineages and B. edulis as a group may specialize on chitin decomposition. Altogether, we show that ecological preferences are likely the primary driver of reproductive barriers in B. edulis.

evolutionary biology↗

bioRxiv2023

Relating Ecological Diversity to Genetic Discontinuity across Bacterial Species

Bacterial genetic discontinuity, representing abrupt breaks in genomic identity among species, is crucial for grasping microbial diversity and evolution. Advances in genomic sequencing have enhanced our ability to track and characterize genetic discontinuity in bacterial populations. However, exploring systematically the degree to which bacterial diversity exists as a continuum or is sorted into discrete and readily defined species remains a challenge in microbial ecology. Here, we aimed to quantify the genetic discontinuity ({delta}) and investigate how this metric is related to ecology. We harnessed a dataset comprising 210,129 genomes to systematically explore genetic discontinuity patterns across several distantly related species, finding clear breakpoints which varied depending on the taxa in question. By delving into pangenome characteristics, we uncovered a significant association between pangenome saturation and genetic discontinuity. Closed pangenomes were associated with more pronounced breaks, exemplified by Mycobacterium tuberculosis. Additionally, through a machine learning approach, we detected key features that impact genetic discontinuity prediction. Our study enhances the understanding of bacterial genetic patterns and their ecological implications, offering insights into species boundaries for prokaryotes.

genomics↗

bioRxiv2023

Disrupted Ecology and H. parainfluenzae Distinguish the Gut Microbiota of an Ethnic Minority Predisposed to Type 2 Diabetes Mellitus

PurposeDecreased gut microbiota production of short-chain fatty acids (SCFAs) has been implicated in type 2 diabetes mellitus (T2DM) disease progression. Most microbiome studies focus on ethnic majorities. This study aims to understand microbiome differences between an ethnic majority (the Dutch) and minority (the South-Asian Surinamese (SAS)) group with a lower and higher prevalence of T2DM, respectively. MethodsMicrobiome data from the Healthy Life in an Urban Setting (HELIUS) cohort were used. The 16S rRNA V4 region was sequenced. Two age- and gender-matched groups were compared: the Dutch (n = 41) and SAS (n = 43). Microbial compositions were generated via DADA2. Alpha and beta-diversity and Principal Coordinate Analysis (PCoA) were computed. DESeq2 differential bacterial abundance and LEfSe biomarker analyses were performed to determine discriminating features. Co-occurrence networks were constructed to examine gut ecology. ResultsA tight cluster of bacterial abundances was observed in the Dutch women, which overlapped with some of the SAS microbiomes. The Dutch gut contained a more interconnected microbial ecology, whereas the SAS network was dispersed. Bacteroides caccae, Butyricicoccus, Alistipes putredinis, Coprococcus comes, Odoribacter splanchnicus, and Lachnospira characterized the Dutch gut. Haemophilus, Bifidobacterium, and Anaerostipes hadrus characterized the SAS gut. All but Lachnospira and certain strains of Haemophilus are known SCFA producers. ConclusionThe Dutch gut microbiome was distinguished from the SAS by diverse, differentially abundant SCFA-producing taxa with significant cooperation. The dynamic ecology observed in the Dutch was lost in the SAS. The higher prevalence of T2DM in the SAS may be associated with the dysbiosis observed.

microbiology↗

bioRxiv2023

Ecological diversification in an adaptive radiation of plants: the role of de novo mutation and introgression

Adaptive radiations are characterized by rapid ecological diversification and speciation events, leading to fuzzy species boundaries between ecologically differentiated species. Adaptive radiations are therefore key systems for understanding how species are formed and maintained, including the role of de novo mutations vs. pre-existing variation in ecological adaptation and the genome-wide consequences of hybridization events. For example, adaptive introgression, where beneficial alleles are transferred between lineages through hybridization, may fuel diversification in adaptive radiations and facilitate adaptation to new environments. In this study, we employed whole-genome resequencing data to investigate the evolutionary origin of hummingbird-pollinated flowers and to characterize genome-wide patterns of phylogenetic discordance and introgression in Penstemon subgenus Dasanthera, a small and diverse adaptive radiation of plants. We found that magenta hummingbird-adapted flowers have apparently evolved twice from ancestral blue-violet bee-pollinated flowers within this radiation. These shifts in flower color are accompanied by a variety of inactivating mutations to a key anthocyanin pathway enzyme, suggesting that independent de novo loss-of-function mutations underlie parallel evolution of this trait. Although patterns of introgression and phylogenetic discordance were heterogenous across the genome, a strong effect of gene density suggests that, in general, natural selection opposes introgression and maintains genetic differentiation in gene-rich genomic regions. Our results highlight the importance of both de novo mutation and introgression as sources of evolutionary change and indicate a role for de novo mutation in driving parallel evolution in adaptive radiations.

evolutionary biology↗

bioRxiv2023

Microbial ecology of coastal northern Gulf of Mexico waters

Estuarine and coastal ecosystems are of high economic and ecological importance, owing to their diverse communities and the disproportionate role they play in carbon cycling, particularly in carbon sequestration. Organisms inhabiting these environments must overcome strong natural fluctuations in salinity, nutrients, and turbidity as well as numerous climate change-induced disturbances such as land loss, sea level rise, and, in some locations, increasingly severe tropical cyclones that threaten to disrupt future ecosystem health. The northern Gulf of Mexico (nGoM) along the Louisiana coast contains dozens of estuaries, including the Mississippi-Atchafalaya River outflow, which dramatically influence the region due to their vast upstream watershed. Nevertheless, the microbiology of these estuaries and surrounding coastal environments have received little attention. To improve our understanding of microbial ecology in the understudied coastal nGoM, we conducted a 16S rRNA gene amplicon survey at eight sites and multiple timepoints along the Louisiana coast and one inland swamp spanning freshwater to high brackish salinities, totaling 47 duplicated Sterivex (0.2-2.7 {micro}m) and prefilter (> 2.7 {micro}m) samples. We cataloged over 13,000 ASVs from common freshwater and marine clades such as SAR11 (Alphaproteobacteria), Synechococcus (Cyanobacteria), and acI and Candidatus Actinomarina (Actinobacteria). We observed preferences for freshwater or marine habitats in many organisms and also characterized a group of taxa with specialized distributions across brackish water sites, supporting the hypothesis of an endogenous brackish-water community. Additionally, we observed brackish-water preferences for several aquatic clades typically considered marine or freshwater taxa, such as SAR11 subclade II, SAR324, and the acI Actinobacteria. The data presented here expand the geographic coverage of microbial ecology in estuarine communities, help delineate the autochthonous and allochthonous members of these environments, and provide critical aquatic microbiological baseline data for coastal and estuarine sites in the nGoM.

microbiology↗

bioRxiv2024

Different metabolite profiles across Penicillium roqueforti populations associated with ecological niche specialisation and domestication

Fungi are known to produce many chemically diversified metabolites, yet their ecological roles are not always fully understood. The blue cheese making fungus Penicillium roqueforti thrives in different ecological niches and is known to produce a wide range of metabolites, including mycotoxins. Three P. roqueforti populations have been domesticated for cheese production and two populations thrive in other anthropized environments, i.e., spoiled food, lumber and silage. Here, we looked for differences in targeted and untargeted metabolite production profiles between populations using HPLC-HR-Q-TOF and UHPLC-Q-TOF-HR-MS/MS. The non-cheese populations produced several fatty acids and different terpenoids, lacking in cheese strains. The Termignon cheese population displayed intermediate metabolite profiles between cheese and non-cheese populations, as previously shown for other traits. The non-Roquefort population, the cheese population with the strongest domestication syndrome, produced the lowest quantities of measured metabolites, including known mycotoxins such as mycophenolic acid (MPA), andrastin A and PR toxin. Its inability to produce MPA was due to a deletion in the mpaC gene, while a premature stop codon in ORF 11 of the PR toxin gene cluster explained its absence and the accumulation of its eremofortin A & B intermediates. In the Roquefort population, we detected no PR toxin nor eremofortins A or B, but found no indel or frameshift mutation, suggesting downregulation. Our results suggest that domesticated cheese populations were selected for lower toxin production while populations from other anthropized environments maintained high metabolite diversity, the bioactivities of these compounds being likely important in these ecological niches.

microbiology↗

bioRxiv2024

Reproductive innovation enabled radiation in the deep sea during an ecological crisis

Major ecological transitions are thought to fuel evolutionary radiations, but whether they are contingent on the evolution of certain traits is unclear. We show that the rapid ecological transition of anglerfishes into pelagic habitats during a period of major global warming coincided with the origins of sexual parasitism, in which male anglerfishes temporarily attach or permanently fuse to females to mate. A phylogenomic reconstruction of the evolutionary history of anglerfishes provides a strong inference for the convergent evolution of permanently-fusing deep-sea anglerfishes and their degenerate immune genes. Our results support that sexual parasitism was enabled by the degeneration of adaptive immunity and ancestral sexual size dimorphism. The combination of these traits facilitated the transition of pelagic anglerfishes into novel ecologies available in the deep open oceans after evolving from benthic ancestors. These results show how seemingly unrelated physiological and reproductive traits interact synergistically to drive evolutionary radiation in novel environments.

evolutionary biology↗

bioRxiv2024

On the ecology of Acinetobacter baumannii - jet stream rider and opportunist by nature

The natural reservoirs of the nosocomial pathogen Acinetobacter baumannii are not well defined. We previously identified white storks as a model system to study the ecology of A. baumannii. Having screened more than 1,300 white stork nestlings over a period of six years across different regions of Poland and Germany (overall isolation rate of [~]29.5%), including food chain analyses and environmental samplings, we come up with a detailed picture of the dynamics and diversity of A. baumannii in their natural habitats. Adult storks, rather than being stably colonized with strains of A. baumannii which are successively transferred to their offspring, instead initially encounter these bacteria while foraging. Among their common food sources, consisting of earthworms, small mammals, and insects, we identified earthworms as a potential source of A. baumannii, but more so the associated soil as well as plant roots. Through this, hotspot soil and compost habitats were identified which enable population dynamics to be studied over the course of the year. We demonstrate that sterilized plant material is rapidly colonized by airborne A. baumannii suggesting they patrol to search for novel habitats, being opportunist by nature. The prevalence of A. baumannii exhibited a strong seasonality and peaked during summer. The strains we collected in Poland and Germany represent more than 50% of the worldwide known diversity in terms of the intrinsic OXA-51-like {beta}-lactamase. A set of [~]400 genomes was determined and compared to a diverse set of publicly available genomes. Our pan-genome estimate of the species ([~]51,000 unique genes) more than doubles the amount proposed by previous studies. Core-genome based phylogenetic analyses illustrated numerous links between wildlife isolates and hospital strains, including ancient as well as recent intercontinental transfer. Our data further suggest massive radiation within the species early after its emergence, matching with human activity during the Neolithic. Deforestation in particular seemed to set the stage for this bloom as we found that forests do not provide conducive conditions for the proliferation of A. baumannii. In contrast, wet and nutrient-rich soil alongside rivers sampled during the summer can yield an isolation rate of [~]30%. Linking published work on the interaction between A. baumannii and fungi and on aspergillosis as a major cause of mortality in white stork nestlings to our findings, we hypothesized that fungi and A. baumannii share a long history of coevolution. Interaction studies revealed the capability of A. baumannii to adhere to fungal spores and to suppress spore germination. Taken together, the intrinsic resistance endowment and potential to acquire antibiotic resistance can be explained by coevolution with antibiotic-producing fungi and other microorganisms within soil, and resistance to desiccation stress and radiation can be interpreted in the light of intercontinental hitchhiking through fungal spores. Originality - SignificanceThe ecology of the nosocomial pathogen Acinetobacter baumannii remains poorly understood outside the hospital. Here, we present the most comprehensive study on its environmental biology to date, after having collected more than 1,450 independent isolates of which around 400 were whole genome-sequenced. This study more than doubles the size of the pan-genome of the species, illustrating both the diversity of our collection and the bias of previous work, but also the bottleneck for the establishment of lineages within the hospital environment. We reached isolation rates of about 30% both in white stork (Ciconia ciconia) nestlings and in soil samples when considering for sampling all preferences of A. baumannii we uncovered. Thus, it is now possible to study the ecology and evolution of A. baumannii in nature at an unprecedented temporal and spatial resolution. We describe the worldwide spread of A. baumannii lineages in nature as an ancient phenomenon that even surpasses that of human-associated bacteria in magnitude. This is likely due to airborne spread, putatively facilitated by association with fungal spores. We propose that A. baumannii is an opportunist by nature, using airborne patrolling to rapidly enter new suitable habitats consisting of organic matter in early stages of decomposition. Our collective data suggest that A. baumannii, early after its speciation, went through massive radiation during the Neolithic, likely due to deforestation, settlement and farming producing numerous favorable habitats. Their natural lifestyle, which requires rapid adaptability to various habitats as well as tolerance to desiccation, radiation and antibiotic stress, perfectly predispose these opportunistic pathogens to establish within the hospital setting. Comparison of genomes from environmental and clinical isolates will now enable studies of the adaptive evolution of environmental bacteria towards multidrug-resistant opportunistic pathogens.

microbiology↗

bioRxiv2024

MetaCompare 2.0: Differential ranking of ecological and human health resistome risks

BackgroundWhile there is increasing recognition of numerous environmental contributions to the spread of antibiotic resistance, quantifying the relative contributions of various sources remains a fundamental challenge. Similarly, there is a need to differentiate acute human health risks corresponding to exposure to a given environment, versus broader ecological risk of evolution and spread of antibiotic resistance genes (ARGs) across microbial taxa. Recent studies have proposed various methods of harnessing the rich information housed by metagenomic data for achieving such aims. Here, we introduce MetaCompare 2.0, which improves upon the original MetaCompare pipeline by differentiating indicators of human health resistome risk (i.e., potential for human pathogens to acquire ARGs) from ecological resistome risk (i.e., overall mobility of ARGs across a given microbiome). ResultsTo demonstrate the sensitivity of the MetaCompare 2.0 pipeline, we analyzed publicly available metagenomes representing a broad array of environments, including wastewater, surface water, soil, sediment, and human gut. We also assessed the effect of sequence assembly methods on the risk scores. We further evaluated the robustness of the pipeline to sequencing depth, contig count, and metagenomic library coverage bias through comparative analysis of a range of subsamples extracted from a set of deeply sequenced wastewater metagenomes. The analysis utilizing samples from different environments demonstrated that MetaCompare 2.0 consistently produces lower risk scores for environments with little human influence and higher risk scores for human contaminated environments affected by pollution or other stressors. We found that the ranks of risk scores were not measurably affected by different assemblers employed. The Meta-Compare 2.0 risk scores were remarkably consistent despite varying sequencing depth, contig count, and coverage. ConclusionMetaCompare 2.0 successfully ranked a wide array of environments according to both human health and ecological resistome risks, with both scores being strongly impacted by anthropogenic stress. We packaged the improved pipeline into a publicly-available web service that provides an easy-to-use interface for computing resistome risk scores and visualizing results. The web service is available at http://metacompare.cs.vt.edu/

bioinformatics↗

bioRxiv2024

Endophytic and ectomycorrhizal, an overlooked dual ecological niche? Insights from natural environments and Russula species

O_LIEctomycorrhizal (EcM) fungi play key roles in ecosystem functioning, in particular temperate ones. Recent findings suggest that they can endophytically colonize the roots of non-EcM plants. Here we aim at (i) providing new evidence of colonization of non-EcM hosts by EcM fungi, (ii) exploring factors driving such colonization (plant identity, site, root filter), and (iii) providing direct microscopical evidence for endophytism. C_LIO_LIUsing amplicon sequencing (ITS2), we described the root fungal communities of 42 plant species collected at nine locations in France. In two of those sites, we also compared rhizosphere and root fungal communities to identify a potential root filter. Finally, we investigated endophytism in Russula spp. at two Russula-rich sites using fluorescence in situ hybridization (FISH) paired with confocal microscopy. C_LIO_LIWe find a large but variable share of EcM sequences in roots of non-EcM plant species, in particular nearby EcM hosts, suggesting that endophytism is a secondary ecological niche. Though EcM fungi were more abundant in the rhizosphere compared to roots, their composition was similar to that of roots, suggesting a poor root filter. We observed metabolically active hyphae of Russula spp. endophytically colonizing the apoplast of two non-EcM plant species. C_LIO_LIAs shown for other EcM fungi (e.g., Tuber spp., Ascomycota) we demonstrate the dual EcM/endophyte niche for Russula (Basidiomycota). The ecological consequences of this duality still need to be addressed. The ability to colonize two ecological niches may be a trait kept by EcM fungi which evolved from endophytic fungi, as stipulated by the "waiting room hypothesis". C_LI

microbiology↗

bioRxiv2024

Bacterial ecology and evolution converge on seasonal and decadal scales

Ecology and evolution are often viewed as distinct processes, which interact on contemporary time scales in microbiomes. To observe these processes in a natural system, we collected a two-decade, 471-sample freshwater lake time series, creating the longest metagenome dataset to date. Among 2,855 species-representative genomes, diverse species and strains followed cyclical seasonal patterns, and one in five species experienced decadal shifts in strain composition. The most globally abundant freshwater bacterium had constant species-level abundance, but environmental extremes appeared to trigger a shift in strain composition and positive selection of amino acid and nucleic acid metabolism genes. These genes identify organic nitrogen compounds as potential drivers of freshwater responses to global change. Seasonal and long-term strain dynamics could be regarded as ecological processes or equivalently as evolutionary change. Rather than as distinct processes that interact, we propose a conceptualization where ecology and evolution converge along a continuum to better describe change in diverse microbial communities.

evolutionary biology↗

bioRxiv2024

Novel misos shape distinct microbial ecologies: opportunities for flavourful sustainable food innovation

Fermentation is resurgent around the world as people seek healthier, more sustainable, and tasty food options. This study explores the microbial ecology of miso, a traditional Japanese fermented paste, made with novel regional substrates to develop new plant-based foods. Eight novel miso varieties were developed using different protein-rich substrates: yellow peas, Gotland lentils, and fava beans (each with two treatments: standard and nixtamalisation), as well as rye bread and soybeans. The misos were produced at Noma, a restaurant in Copenhagen, Denmark. Samples were analysed with biological and technical triplicates at the beginning and end of fermentation. We also incorporated in this study six samples of novel misos produced following the same recipe at Inua, a former affiliate restaurant of Noma in Tokyo, Japan. To analyse microbial community structure and diversity, metabarcoding (16S and ITS) and shotgun metagenomic analyses were performed. The misos contain a greater range of microbes than is currently described for miso in the literature. The composition of the novel yellow pea misos was notably similar to the traditional soybean ones, suggesting they are a good alternative, which supports our culinary collaborators sensory conclusions. For bacteria, we found that overall substrate had the strongest effect, followed by time, treatment (nixtamalisation), and geography. For fungi, there was a slightly stronger effect of geography and a mild effect of substrate, and no significant effects for treatment or time. Based on an analysis of metagenome-assembled genomes (MAGs), strains of S. epidermidis differentiated according to substrate. Carotenoid biosynthesis genes in these MAGs appeared in strains from Japan but not from Denmark, suggesting a possible gene-level geographical effect. The benign and possibly functional presence of S. epidermidis in these misos, a species typically associated with the human skin microbiome, suggests possible adaptation to the miso niche, and the flow of microbes between bodies and foods in certain fermentation as more common than is currently recognised. This study improves our understanding of miso ecology, highlights the potential for developing novel misos using diverse local ingredients, and suggests how fermentation innovation can contribute to studies of microbial ecology and evolution.

microbiology↗