Synthesis of recovery patterns in microbial communities across environments.

BACKGROUND: Disturbances alter the diversity and composition of microbial communities. Yet a generalized empirical assessment of microbiome responses to disturbance across different environments is needed to understand the factors driving microbiome recovery, and the role of the environment in driving these patterns. RESULTS: To this end, we combined null models with Bayesian generalized linear models to examine 86 time series of disturbed mammalian, aquatic, and soil microbiomes up to 50 days following disturbance. Overall, disturbances had the strongest effect on mammalian microbiomes, which lost taxa and later recovered their richness, but not their composition. In contrast, following disturbance, aquatic microbiomes tended away from their pre-disturbance composition over time. Surprisingly, across all environments, we found no evidence of increased compositional dispersion (i.e., variance) following disturbance, in contrast to the expectations of the Anna Karenina Principle. CONCLUSIONS: This is the first study to systematically compare secondary successional dynamics across disturbed microbiomes, using a consistent temporal scale and modeling approach. Our findings show that the recovery of microbiomes is environment-specific, and helps to reconcile existing, environment-specific research into a unified perspective. Video Abstract.

Erratum: Universal drivers of cheese microbiomes.

[This corrects the article DOI: 10.1016/j.isci.2022.105744.].

Datathons: fostering equitability in data reuse in ecology.

Approaches to rapidly collecting global biodiversity data are increasingly important, but biodiversity blind spots persist. We organized a three-day Datathon event to improve the openness of local biodiversity data and facilitate data reuse by local researchers. The first Datathon, organized among microbial ecologists in Uruguay and Argentina assembled the largest microbiome dataset in the region to date and formed collaborative consortia for microbiome data synthesis.

The AnimalAssociatedMetagenomeDB reveals a bias towards livestock and developed countries and blind spots in functional-potential studies of animal-associated microbiomes.

BACKGROUND: Metagenomic data can shed light on animal-microbiome relationships and the functional potential of these communities. Over the past years, the generation of metagenomics data has increased exponentially, and so has the availability and reusability of data present in public repositories. However, identifying which datasets and associated metadata are available is not straightforward. We created the Animal-Associated Metagenome Metadata Database (AnimalAssociatedMetagenomeDB - AAMDB) to facilitate the identification and reuse of publicly available non-human, animal-associated metagenomic data, and metadata. Further, we used the AAMDB to (i) annotate common and scientific names of the species; (ii) determine the fraction of vertebrates and invertebrates; (iii) study their biogeography; and (iv) specify whether the animals were wild, pets, livestock or used for medical research. RESULTS: We manually selected metagenomes associated with non-human animals from SRA and MG-RAST.  Next, we standardized and curated 51 metadata attributes (e.g., host, compartment, geographic coordinates, and country). The AAMDB version 1.0 contains 10,885 metagenomes associated with 165 different species from 65 different countries. From the collected metagenomes, 51.1% were recovered from animals associated with medical research or grown for human consumption (i.e., mice, rats, cattle, pigs, and poultry). Further, we observed an over-representation of animals collected in temperate regions (89.2%) and a lower representation of samples from the polar zones, with only 11 samples in total. The most common genus among invertebrate animals was Trichocerca (rotifers). CONCLUSION: Our work may guide host species selection in novel animal-associated metagenome research, especially in biodiversity and conservation studies. The data available in our database will allow scientists to perform meta-analyses and test new hypotheses (e.g., host-specificity, strain heterogeneity, and biogeography of animal-associated metagenomes), leveraging existing data. The AAMDB WebApp is a user-friendly interface that is publicly available at https://webapp.ufz.de/aamdb/ .

COVID-19 alters human microbiomes: a meta-analysis.

Introduction: Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) has infected a substantial portion of the world's population, and novel consequences of COVID-19 on the human body are continuously being uncovered. The human microbiome plays an essential role in host health and well-being, and multiple studies targeting specific populations have reported altered microbiomes in patients infected with SARS-CoV-2. Given the global scale and massive incidence of COVID on the global population, determining whether the effects of COVID-19 on the human microbiome are consistent and generalizable across populations is essential. Methods: We performed a synthesis of human microbiome responses to COVID-19. We collected 16S rRNA gene amplicon sequence data from 11 studies sampling the oral and nasopharyngeal or gut microbiome of COVID-19-infected and uninfected subjects. Our synthesis included 1,159 respiratory (oral and nasopharyngeal) microbiome samples and 267 gut microbiome samples from patients in 11 cities across four countries. Results: Our reanalyses revealed communitywide alterations in the respiratory and gut microbiomes across human populations. We found significant overall reductions in the gut microbial diversity of COVID-19-infected patients, but not in the respiratory microbiome. Furthermore, we found more consistent community shifts in the gut microbiomes of infected patients than in the respiratory microbiomes, although the microbiomes in both sites exhibited higher host-to-host variation in infected patients. In respiratory microbiomes, COVID-19 infection resulted in an increase in the relative abundance of potentially pathogenic bacteria, including Mycoplasma. Discussion: Our findings shed light on the impact of COVID-19 on the human-associated microbiome across populations, and highlight the need for further research into the relationship between long-term effects of COVID-19 and altered microbiota.

The heterogeneity-diversity-system performance nexus.

Ever-growing human population and nutritional demands, supply chain disruptions, and advancing climate change have led to the realization that changes in diversity and system performance are intimately linked. Moreover, diversity and system performance depend on heterogeneity. Mitigating changes in system performance and promoting sustainable living conditions requires transformative decisions. Here, we introduce the heterogeneity-diversity-system performance (HDP) nexus as the conceptual basis upon which to formulate transformative decisions. We suggest that managing the heterogeneity of systems will best allow diversity to provide multiple benefits to people. Based on ecological theory, we pose that the HDP nexus is broadly applicable across systems, disciplines, and sectors, and should thus be considered in future decision making as a way to have a more sustainable global future.

Beyond pathogenesis: Detecting the full spectrum of ecological interactions in the virosphere.

The public perception of viruses has historically been negative. We are now at a stage where the development of tools to study viruses is at an all-time high, but society's perception of viruses is at an all-time low. The literature regarding viral interactions has been skewed towards negative (i.e., pathogenic) symbioses, whereas viral mutualisms remain relatively underexplored. Viral interactions with their hosts are complex and some non-pathogenic viruses could have potential benefits to society. However, viral research is seldom designed to identify viral mutualists, a gap that merits considering new experimental designs. Determining whether antagonisms, mutualisms, and commensalisms are equally common ecological strategies requires more balanced research efforts that characterize the full spectrum of viral interactions.

Universal drivers of cheese microbiomes.

The culinary value, quality, and safety of cheese are largely driven by the resident bacteria, but comparative analyses of the cheese microbiota across cheese types are scarce. We present the first global synthesis of cheese microbiomes. Following a systematic literature review of cheese microbiology research, we collected 16S rRNA gene amplicon sequence data from 824 cheese samples spanning 58 cheese types and 16 countries. We found a consistent, positive relationship between microbiome richness and pH, and a higher microbial richness in cheeses derived from goat milk. In contrast, we found no relationship between pasteurization, geographic location, or salinity and richness. Milk and cheese type, geographic location, and pasteurization collectively explained 65% of the variation in microbial community composition. Importantly, we identified four universal cheese microbiome types, driven by distinct dominant taxa. Our study reveals notable diversity patterns among the cheese microbiota, which are driven by geography and local environmental variables.

The community ecology perspective of omics data.

The measurement of uncharacterized pools of biological molecules through techniques such as metabarcoding, metagenomics, metatranscriptomics, metabolomics, and metaproteomics produces large, multivariate datasets. Analyses of these datasets have successfully been borrowed from community ecology to characterize the molecular diversity of samples (ɑ-diversity) and to assess how these profiles change in response to experimental treatments or across gradients (ß-diversity). However, sample preparation and data collection methods generate biases and noise which confound molecular diversity estimates and require special attention. Here, we examine how technical biases and noise that are introduced into multivariate molecular data affect the estimation of the components of diversity (i.e., total number of different molecular species, or entities; total number of molecules; and the abundance distribution of molecular entities). We then explore under which conditions these biases affect the measurement of ɑ- and ß-diversity and highlight how novel methods commonly used in community ecology can be adopted to improve the interpretation and integration of multivariate molecular data. Video Abstract.

Succession in the caecal microbiota of developing broilers colonised by extended-spectrum ß-lactamase-producing Escherichia coli.

BACKGROUND: Broilers are among the most common and dense poultry production systems, where antimicrobials have been used extensively to promote animal health and performance. The continuous usage of antimicrobials has contributed to the appearance of resistant bacteria, such as extended-spectrum ß-lactamase-producing Escherichia coli (ESBL-Ec). Here, we studied the ESBL-Ec prevalence and successional dynamics of the caecal microbiota of developing broilers in a commercial flock during their production life cycle (0-35 days). Broilers were categorised as ESBL-Ec colonised (ESBL-Ec+) or ESBL-Ec non-colonised (ESBL-Ec-) by selective culturing. Using 16S rRNA gene sequencing, we i. compared the richness, evenness and composition of the caecal microbiota of both broilers' groups and ii. assessed the combined role of age and ESBL-Ec status on the broilers' caecal microbiota. RESULTS: From day two, we observed an increasing linear trend in the proportions of ESBL-Ec throughout the broilers' production life cycle, X2 (1, N = 12) = 28.4, p < 0.001. Over time, the caecal microbiota richness was consistently higher in ESBL-Ec- broilers, but significant differences between both broilers' groups were found exclusively on day three (Wilcoxon rank-sum test, p = 0.016). Bray-Curtis distance-based RDA (BC-dbRDA) showed no explanatory power of ESBL-Ec status, while age explained 14% of the compositional variation of the caecal microbiota, F (2, 66) = 6.47, p = 0.001. CONCLUSIONS: This study assessed the role of ESBL-Ec in the successional dynamics of the caecal microbiota in developing broilers and showed that the presence of ESBL-Ec is associated with mild but consistent reductions in alpha diversity and with transient bacterial compositional differences. We also reported the clonal spread of ESBL-Ec and pointed to the farm environment as a likely source for ESBLs.

All together now: Limitations and recommendations for the simultaneous analysis of all eukaryotic soil sequences.

The soil environment contains a large, but historically underexplored, reservoir of biodiversity. Sequencing prokaryotic marker genes has become commonplace for the discovery and characterization of soil bacteria and archaea. Increasingly, this approach is also applied to eukaryotic marker genes to characterize the diversity and distribution of soil eukaryotes. However, understanding the properties and limitations of eukaryotic marker sequences is essential for correctly analysing, interpreting, and synthesizing the resulting data. Here, we illustrate several biases from sequencing data that affect measurements of biodiversity that arise from variation in morphology, taxonomy and phylogeny between organisms, as well as from sampling designs. We recommend analytical approaches to overcome these limitations, and outline how the benchmarking and standardization of sequencing protocols may improve the comparability of the data.

Age Matters: Community Assembly in the Pig Fecal Microbiome in the First Month of Life.

Despite the wealth of research into strategies for microbiome modulation, studies of microbiome management in pig hosts have found mixed results. A refined understanding of the patterns of microbiome assembly during the host's early life, when management strategies are most commonly applied, is necessary for the development of successful management practices. Here, we study the development of the pig gut microbial community in a monitoring experiment, sampling the microbiome of pigs in a commercial farm intensively during the first month of life. We found that the community's taxonomic richness increased linearly with host age. Furthermore, rapid changes across communities occurred in stages, and non-linear patterns in relative abundance were commonly observed among dominant taxa across host age, consistent with primary succession. Our results highlight the importance of understanding the patterns of microbiome assembly during host development, and identify successional stages as windows of opportunity for future research.

The multidimensionality of soil macroecology.

The recent past has seen a tremendous surge in soil macroecological studies and new insights into the global drivers of one-quarter of the biodiversity of the Earth. Building on these important developments, a recent paper in Global Ecology and Biogeography outlined promising methods and approaches to advance soil macroecology. Among other recommendations, White and colleagues introduced the concept of a spatial three-dimensionality in soil macroecology by considering the different spheres of influence and scales, as soil organism size ranges vary from bacteria to macro- and megafauna. Here, we extend this concept by discussing three additional dimensions (biological, physical, and societal) that are crucial to steer soil macroecology from pattern description towards better mechanistic understanding. In our view, these are the requirements to establish it as a predictive science that can inform policy about relevant nature and management conservation actions. We highlight the need to explore temporal dynamics of soil biodiversity and functions across multiple temporal scales, integrating different facets of biodiversity (i.e., variability in body size, life-history traits, species identities, and groups of taxa) and their relationships to multiple ecosystem functions, in addition to the feedback effects between humans and soil biodiversity. We also argue that future research needs to consider effective soil conservation policy and management in combination with higher awareness of the contributions of soil-based nature's contributions to people. To verify causal relationships, soil macroecology should be paired with local and globally distributed experiments. The present paper expands the multidimensional perspective on soil macroecology to guide future research contents and funding. We recommend considering these multiple dimensions in projected global soil biodiversity monitoring initiatives.

Tree diversity and soil chemical properties drive the linkages between soil microbial community and ecosystem functioning.

Microbial respiration is critical for soil carbon balance and ecosystem functioning. Previous studies suggest that plant diversity influences soil microbial communities and their respiration. Yet, the linkages between tree diversity, microbial biomass, microbial diversity, and microbial functioning have rarely been explored. In this study, we measured two microbial functions (microbial physiological potential, and microbial respiration), together with microbial biomass, microbial taxonomic and functional profiles, and soil chemical properties in a tree diversity experiment in South China, to disentangle how tree diversity affects microbial respiration through the modifications of the microbial community. Our analyses show a significant positive effect of tree diversity on microbial biomass (+25% from monocultures to 24-species plots), bacterial diversity (+12%), and physiological potential (+12%). In addition, microbial biomass and physiological potential, but not microbial diversity, were identified as the key drivers of microbial respiration. Although soil chemical properties strongly modulated soil microbial community, tree diversity increased soil microbial respiration by increasing microbial biomass rather than changing microbial taxonomic or functional diversity. Overall, our findings suggest a prevalence of microbial biomass over diversity in controlling soil carbon dynamics.

The archives are half-empty: an assessment of the availability of microbial community sequencing data.

As DNA sequencing has become more popular, the public genetic repositories where sequences are archived have experienced explosive growth. These repositories now hold invaluable collections of sequences, e.g., for microbial ecology, but whether these data are reusable has not been evaluated. We assessed the availability and state of 16S rRNA gene amplicon sequences archived in public genetic repositories (SRA, EBI, and DDJ). We screened 26,927 publications in 17 microbiology journals, identifying 2015 16S rRNA gene sequencing studies. Of these, 7.2% had not made their data public at the time of analysis. Among a subset of 635 studies sequencing the same gene region, 40.3% contained data which was not available or not reusable, and an additional 25.5% contained faults in data formatting or data labeling, creating obstacles for data reuse. Our study reveals gaps in data availability, identifies major contributors to data loss, and offers suggestions for improving data archiving practices.

Soil microbial composition varies in response to coffee agroecosystem management.

Soil microbes are essential to the continued productivity of sustainably managed agroecosystems. In shade coffee plantations, the relationship between soil microbial composition, soil nutrient availability and coffee productivity have been demonstrated, but the effects of management on the composition of the soil microbial communities remains relatively unexplored. To further understand how management modulates the soil microbiome, the soil fungal and bacterial communities, soil chemistry, and canopy composition were surveyed in a Nicaraguan coffee cooperative, across 19 individual farms. Amplicon sequencing analyses showed that management (organic or conventional), stand age and previous land use affected the soil microbiome, albeit in different ways. Bacterial communities were most strongly associated with soil chemistry, while fungal communities were more strongly associated with the composition of the canopy and historical land use of the coffee plantation. Notably, both fungal and bacterial richness decreased with stand age. In addition to revealing the first in-depth characterization of the soil microbiome in coffee plantations in Nicaragua, these results highlight how fungal and bacterial communities are simultaneously modulated by long-term land use legacies (i.e. an agricultural plot's previous land use) and short-term press disturbance (i.e. farm age).

An observational field study of the cloacal microbiota in adult laying hens with and without access to an outdoor range.

BACKGROUND: Laying hens with access to outdoor ranges are exposed to additional environmental factors and microorganisms, including potential pathogens. Differences in composition of the cloacal microbial community between indoor- and outdoor-housed layers may serve as an indicator for exposure to the outdoor environment, including its pathogens, and may yield insights into factors affecting the chickens' microbiota community dynamics. However, little is known about the influence of outdoor housing on microbiota community composition in commercial layer flocks. We performed a cross-sectional field study to evaluate differences in the cloacal microbiota of indoor- vs outdoor-layers across farms. Eight layer flocks (four indoor, four outdoor) from five commercial poultry farms were sampled. Indoor and outdoor flocks with the same rearing flock of origin, age, and breed were selected. In each flock, cloacal swabs were taken from ten layers, and microbiota were analysed with 16S rRNA gene amplicon sequencing. RESULTS: Housing type (indoor vs outdoor), rearing farm, farm and poultry house within the farm all significantly contributed to bacterial community composition. Poultry house explained most of the variation (20.9%), while housing type only explained 0.2% of the variation in community composition. Bacterial diversity was higher in indoor-layers than in outdoor-layers, and indoor-layers also had more variation in their bacterial community composition. No phyla or genera were found to be differentially abundant between indoor and outdoor poultry houses. One amplicon sequence variant was exclusively present in outdoor-layers across all outdoor poultry houses, and was identified as Dietzia maris. CONCLUSIONS: This study shows that exposure to an outdoor environment is responsible for a relatively small proportion of the community variation in the microbiota of layers. The poultry house, farm, and rearing flock play a much greater role in determining the cloacal microbiota composition of adult laying hens. Overall, measuring differences in cloacal microbiota of layers as an indicator for the level of exposure to potential pathogens and biosecurity seems of limited practical use. To gain more insight into environmental drivers of the gut microbiota, future research should aim at investigating community composition of commercial layer flocks over time.

Temporal Dynamics of Cloacal Microbiota in Adult Laying Chickens With and Without Access to an Outdoor Range.

Associations between animal health and performance, and the host's microbiota have been recently established. In poultry, changes in the intestinal microbiota have been linked to housing conditions and host development, but how the intestinal microbiota respond to environmental changes under farm conditions is less well understood. To gain insight into the microbial responses following a change in the host's immediate environment, we monitored four indoor flocks of adult laying chickens three times over 16 weeks, during which two flocks were given access to an outdoor range, and two were kept indoors. To assess changes in the chickens' microbiota over time, we collected cloacal swabs of 10 hens per flock and performed 16S rRNA gene amplicon sequencing. The poultry house (i.e., the stable in which flocks were housed) and sampling time explained 9.2 and 4.4% of the variation in the microbial community composition of the flocks, respectively. Remarkably, access to an outdoor range had no detectable effect on microbial community composition, the variability of microbiota among chickens of the same flock, or microbiota richness, but the microbiota of outdoor flocks became more even over time. Fluctuations in the composition of the microbiota over time within each poultry house were mainly driven by turnover in rare, rather than dominant, taxa and were unique for each flock. We identified 16 amplicon sequence variants that were differentially abundant over time between indoor and outdoor housed chickens, however none were consistently higher or lower across all chickens of one housing type over time. Our study shows that cloacal microbiota community composition in adult layers is stable following a sudden change in environment, and that temporal fluctuations are unique to each flock. By exploring microbiota of adult poultry flocks within commercial settings, our study sheds light on how the chickens' immediate environment affects the microbiota composition.

Limited changes in the fecal microbiome composition of laying hens after oral inoculation with wild duck feces.

Interspecies transmission of fecal microbiota can serve as an indicator for (indirect) contact between domestic and wild animals to assess risks of pathogen transmission, e.g., avian influenza. Here, we investigated whether oral inoculation of laying hens with feces of wild ducks (mallards, Anas platyrhynchos) resulted in a hen fecal microbiome that was detectably altered on community parameters or relative abundances of individual genera. To distinguish between effects of the duck inoculum and effects of the inoculation procedure, we compared the fecal microbiomes of adult laying hens resulting from 3 treatments: inoculation with wild duck feces (duck), inoculation with chicken feces (auto), and a negative control group with no treatment. We collected cloacal swabs from 7 hens per treatment before (day 0), and 2 and 7 D after inoculation, and performed 16S rRNA amplicon sequencing. No distinguishable effect of inoculation with duck feces on microbiome community (alpha and beta diversity) was found compared to auto or control treatments. At the individual taxonomic level, the relative abundance of the genus Alistipes (phylum Bacteroidetes) was significantly higher in the inoculated treatments (auto and duck) compared to the control 2 D after inoculation. Seven days after inoculation, the relative abundance of Alistipes had increased in the control and no effect was found anymore across treatments. These effects might be explained by the perturbation of the hen's microbiome caused by the inoculation procedure itself, or by intrinsic temporal variation in the hen's microbiome. This experiment shows that a single inoculation of fecal microbiota from duck feces to laying hens did not cause a measurable alteration of the gut microbiome community. Furthermore, the temporary change in relative abundance for Alistipes could not be attributed to the duck feces inoculation. These outcomes suggest that the fecal microbiome of adult laying hens may not be a useful indicator for detection of single oral exposure to wild duck feces.