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A review of asteroid biology in the context of sea star wasting: Possible causes and consequences

Sea star wasting—marked in a variety of sea star species as varying degrees of skin lesions followed by disintegration—recently caused one of the largest marine die-offs ever recorded on the west coast of North America, killing billions of sea stars. Despite the important ramifications this mortality had for coastal benthic ecosystems, such as increased abundance of prey, little is known about the causes of the disease or the mechanisms of its progression. Although there have been studies indicating a range of causal mechanisms, including viruses and environmental effects, the broad spatial and depth range of affected populations leaves many questions remaining about either infectious or non-infectious mechanisms. Wasting appears to start with degradation of mutable connective tissue in the body wall, leading to disintegration of the epidermis. Here, we briefly review basic sea star biology in the context of sea star wasting and present our current knowledge and hypotheses related to the symptoms, the microbiome, the viruses, and the associated environmental stressors. We also highlight throughout the article knowledge gaps and the data needed to better understand sea star wasting mechanistically, its causes, and potential management.

Biological Bulletin

A decade of death and other dynamics: Deepening perspectives on the diversity and distribution of sea stars and wasting

Mass mortality events provide valuable insight into biological extremes and also ecological interactions more generally. The sea star wasting epidemic that began in 2013 catalyzed study of the microbiome, genetics, population dynamics, and community ecology of several high-profile species inhabiting the northeastern Pacific but exposed a dearth of information on the diversity, distributions, and impacts of sea star wasting for many lesser-known sea stars and a need for integration across scales. Here, we combine datasets from single-site to coast-wide studies, across time lines from weeks to decades, for 65 species. We evaluated the impacts of abiotic characteristics hypothetically associated with sea star wasting (sea surface temperature, pelagic primary productivity, upwelling wind forcing, wave exposure, freshwater runoff) and species characteristics (depth distribution, developmental mode, diet, habitat, reproductive period). We find that the 2010s sea star wasting outbreak clearly affected a little over a dozen species, primarily intertidal and shallow subtidal taxa, causing instantaneous wasting prevalence rates of 5%–80%. Despite the collapse of some populations within weeks, environmental and species variation protracted the outbreak, which lasted 2–3 years from onset until declining to chronic background rates of ∼2% sea star wasting prevalence. Recruitment began immediately in many species, and in general, sea star assemblages trended toward recovery; however, recovery was heterogeneous, and a marine heatwave in 2019 raised concerns of a second decline. The abiotic stressors most associated with the 2010s sea star wasting outbreak were elevated sea surface temperature and low wave exposure, as well as freshwater discharge in the north. However, detailed data speaking directly to the biological, ecological, and environmental cause(s) and consequences of the sea star wasting outbreak remain limited in scope, unavoidably retrospective, and perhaps always indeterminate. Redressing this shortfall for the future will require a broad spectrum of monitoring studies not less than the taxonomically broad cross-scale framework we have modeled in this synthesis.

Biological Bulletin

A global perspective on bacterial diversity in the terrestrial deep subsurface

While recent efforts to catalogue Earth’s microbial diversity have focused upon surface and marine habitats, 12–20 % of Earth’s biomass is suggested to exist in the terrestrial deep subsurface, compared to ~1.8 % in the deep subseafloor. Metagenomic studies of the terrestrial deep subsurface have yielded a trove of divergent and functionally important microbiomes from a range of localities. However, a wider perspective of microbial diversity and its relationship to environmental conditions within the terrestrial deep subsurface is still required. Our meta-analysis reveals that terrestrial deep subsurface microbiota are dominated by Betaproteobacteria, Gammaproteobacteria and Firmicutes , probably as a function of the diverse metabolic strategies of these taxa. Evidence was also found for a common small consortium of prevalent Betaproteobacteria and Gammaproteobacteria operational taxonomic units across the localities. This implies a core terrestrial deep subsurface community, irrespective of aquifer lithology, depth and other variables, that may play an important role in colonizing and sustaining microbial habitats in the deep terrestrial subsurface. An in silico contamination-aware approach to analysing this dataset underscores the importance of downstream methods for assuring that robust conclusions can be reached from deep subsurface-derived sequencing data. Understanding the global panorama of microbial diversity and ecological dynamics in the deep terrestrial subsurface provides a first step towards understanding the role of microbes in global subsurface element and nutrient cycling.

Microbiology

Ecological acclimation: A framework to integrate fast and slow responses to climate change

Ecological responses to climate change occur across vastly different time-scales, from minutes for physiological plasticity to decades or centuries for community turnover and evolutionary adaptation. Accurately predicting the range of ecosystem trajectories will require models that incorporate both fast processes that may keep pace with climate change and slower ones likely to lag behind and generate disequilibrium dynamics. However, the knowledge necessary for this integration is currently fragmented across disciplines. We develop ‘ecological acclimation’ as a unifying framework to emphasize the similarity of dynamics driven by processes operating on dramatically different time-scales and levels of biological organization. The framework focuses on ecoclimate sensitivities, measured as the change in an ecological response variable per unit of climate change. Acclimation processes acting at different time-scales cause these sensitivities to shift in magnitude and even direction over time. We highlight shifting ecoclimate sensitivities in case studies from diverse ecosystems, including terrestrial plant communities, coral reefs and soil microbiomes. Models predicting future ecosystem states inevitably make assumptions about acclimation processes; these assumptions must be explicit for users to evaluate whether a model is appropriate for a given forecast horizon. Similarly, decision frameworks that clearly account for multiple acclimation processes and their distinct time-scales will help natural resource managers plan for ecological impacts of climate change from years to many decades into the future. We outline a synthetic research programme focused on the time-scales of ecological acclimation to reduce uncertainty in ecological forecasts.

Functional Ecology

Epigenetics in captivity: Restoring wild phenotypes in captive-reared salmonids

Captive rearing is a common practice for the stocking, conservation, and supplementation of fish species worldwide, but captive-reared fish can exhibit altered phenotypes leading to reduced fitness in nature compared to wild conspecifics. In salmonids, certain studies have found limited genetic differentiation between wild and captive-reared fish. However, documented changes in gene expression in hatchery fish have led scientists to investigate epigenetic mechanisms, such as DNA methylation, as a source of these differences. In this binational collaborative piece, we synthesize the knowledge and efforts of academics and government scientists to highlight how interactions between captive rearing and the epigenome elicit parallel phenotypic changes across salmonid species. We examine the known and potential links between DNA methylation and the phenotypic effects of captive rearing including changes in behavior, color, gut microbiomes, and developmental abnormalities. We review efforts to minimize these phenotypic and epigenetic effects including attempts to modify the hatchery environment and rearing protocols. We provide a framework to integrate epigenetic considerations into hatchery rearing protocols by weighing the heritable nature of DNA methylation with the goals of different captive rearing programs and explore whether minimizing the phenotypic and epigenetic effects of captive rearing is worthwhile. We examine heritability and persistence of epigenetic effects, and we propose the exploitation of heritable bet-hedging as an epigenetic buffer to increase post-release survival. We also suggest novel applications of epigenomic biomarkers as a non-lethal method for post-release monitoring. Ultimately, collaborative multi-disciplinary research across species is needed to understand the comprehensive effects of captive rearing, reduce the ecological impacts of captive fish in the wild, and increase population resilience. Integrating epigenetics into fish hatchery management will provide new opportunities for optimizing and improving captive rearing.

Evolutionary Applications

Threats posed by the Fungal Kingdom to humans, wildlife, and agriculture

The Fungal Kingdom includes at least six million eukaryotic species and is remarkable with respect to its profound impact on global health, biodiversity, ecology, agriculture, manufacturing, and biomedical research. Approximately 625 fungal species have been reported to infect vertebrates, 200 of which can be human-associated, either as commensals and members of our microbiome or as pathogens that cause infectious diseases. These organisms pose a growing threat to human health with the global increase in the incidence of invasive fungal infections, prevalence of fungal allergy, and the evolution of fungal pathogens resistant to some or all current classes of antifungals. More broadly, there has been an unprecedented and worldwide emergence of fungal pathogens impacting animal and plant biodiversity. Approximately 8,000 species of fungi and Oomycetes are associated with plant disease. Indeed, across agriculture, such fungal diseases of plants include new devastating epidemics of trees and jeopardize food security worldwide by causing epidemics in staple and commodity crops that feed billions. Further, ingestion of mycotoxins contributes to ill health and causes cancer. Coordinated international research efforts, enhanced technology translation, and greater policy outreach by scientists are needed to more fully understand the biology and drivers that underlie the emergence of fungal diseases and to mitigate against their impacts. Here, we focus on poignant examples of emerging fungal threats in each of three areas: human health, wildlife biodiversity, and food security.

mBio

Krumholzibacteriota and Deltaproteobacteria contain rare genetic potential to liberate carbon from monoaromatic compounds in subsurface coal seams

Biogenic methane in subsurface coal seam environments is produced by diverse consortia of microbes. Although this methane is useful for global energy security, it remains unclear which microbes can liberate carbon from the coal. Most of this carbon is relatively resistant to biodegradation, as it is contained within aromatic rings. Thus, to explore for coal-degrading taxa in the subsurface, this study reconstructed relevant metagenome-assembled genomes (MAGs) from coal seams by using a key genomic marker for the anaerobic degradation of monoaromatic compounds as a guide: the benzoyl-CoA reductase gene ( bcrABCD ). Three MAGs were identified with this genetic potential. The first represented a novel taxon from the Krumholzibacteriota phylum, which this study is the first to describe. This Krumholzibacteriota MAG contained a full set of genes for benzoyl-CoA dearomatization, in addition to other genes for anaerobic catabolism of monoaromatics. Analysis of Krumholzibacteriota MAGs from other environments revealed that this genetic potential may be common, and thus, Krumholzibacteriota may be important organisms for the liberation of recalcitrant carbon in a broad range of environments. Moreover, the assembly and characterization of two Syntrophorhabdus aromaticivorans MAGs from different continents and a Syntrophaceae sp. MAG implicate the Deltaproteobacteria class in coal seam monoaromatic degradation. Each of these taxa are potential rate-limiting organisms for subsurface coal-to-methane biodegradation. Their description here provides some understanding of their function within the coal seam microbiome and will help inform future efforts in coal bed methane stimulation, anoxic bioremediation of organic pollutants, and assessments of anoxic, subsurface carbon cycling and emissions.

mBio

Mycobiome traits associated with disease tolerance predict many western North American bat species will be susceptible to white-nose syndrome

White-nose syndrome (WNS), a fungal disease that has caused catastrophic population declines of bats in eastern North America, is rapidly spreading across the continent and now threatens previously unexposed bat species in western North America. The causal agent of WNS, the fungus Pseudogymnoascus destructans , can infect many species of hibernating bats, but susceptibility to WNS varies by host species. We previously reported that certain traits of the skin microbiome, particularly yeast diversity and abundance, of bat species in eastern North America are strongly associated with resistance to WNS. Using these traits, we developed models to predict WNS susceptibility of 13 species of western North American bats. Based on models derived from yeast species diversity, only one bat species, Myotis velifer , was predicted to be WNS resistant (i.e., may develop the disease, but with low mortality rates). We also screened yeasts found on western bats for P. destructans -antagonistic properties by spore germination and growth inhibition/competition assays and found the ability of yeasts to inhibit P. destructans in vitro to be strain specific. Similar to results of inhibition assays performed with yeasts isolated from bats in eastern North America, few yeasts isolated from bats in western North America inhibited P. destructans in vitro. Continued monitoring of western bat populations will serve to validate the accuracy of the mycobiome analysis in predicting WNS susceptibility, document population and susceptibility trends, and identify additional predictors to assess the vulnerability of naive bat populations to WNS.

Microbilogy Spectrum

Resistance, resilience, and recovery of dryland soil bacterial communities across multiple disturbances

Dryland ecosystems are sensitive to perturbations and generally slow to recover post disturbance. The microorganisms residing in dryland soils are especially important as they contribute to soil structure and nutrient cycling. Disturbance can have particularly strong effects on dryland soil structure and function, yet the natural resistance and recovery of the microbial components of dryland soils has not been well documented. In this study, the recovery of surface soil bacterial communities from multiple physical and environmental disturbances is assessed. Samples were collected from three field sites in the vicinity of Moab, UT, United States, 6 to 7 years after physical and climate disturbance manipulations had been terminated, allowing for the assessment of community recovery. Additionally, samples were collected in a transect that included three habitat patches: the canopy zone soils under the dominant shrubs, the interspace soils that are colonized by biological soil crusts, and edge soils at the plot borders. Field site and habitat patch were significant factors structuring the bacterial communities, illustrating that sites and habitats harbored unique soil microbiomes. Across the different sites and disturbance treatments, there was evidence of significant bacterial community recovery, as bacterial biomass and diversity were not significantly different than control plots. There was, however, a small number of 16S rRNA gene amplicon sequence variants that distinguished particular treatments, suggesting that legacy effects of the disturbances still remained. Taken together, these data suggest that dryland bacterial communities may possess a previously unappreciated potential to recover within years of the original disturbance.

Frontiers in Microbiology

Probiotics beyond the farm: Benefits, costs, and considerations of using antibiotic alternatives in livestock

The increasing global expansion of antimicrobial resistant infections warrants the development of effective antibiotic alternative therapies, particularly for use in livestock production, an agricultural sector that is perceived to disproportionately contribute to the antimicrobial resistance (AMR) crisis by consuming nearly two-thirds of the global antibiotic supply. Probiotics and probiotic derived compounds are promising alternative therapies, and their successful use in disease prevention, treatment, and animal performance commands attention. However, insufficient or outdated probiotic screening techniques may unintentionally contribute to this crisis, and few longitudinal studies have been conducted to determine what role probiotics play in AMR dissemination in animal hosts and the surrounding environment. In this review, we briefly summarize the current literature regarding the efficacy, feasibility, and limitations of probiotics, including an evaluation of their impact on the animal microbiome and resistome and their potential to influence AMR in the environment. Probiotic application for livestock is often touted as an ideal alternative therapy that might reduce the need for antibiotic use in agriculture and the negative downstream impacts. However, as detailed in this review, limited research has been conducted linking probiotic usage with reductions in AMR in agricultural or natural environments. Additionally, we discuss the methods, including limitations, of current probiotic screening techniques across the globe, highlighting approaches aimed at reducing antibiotic usage and ensuring safe and effective probiotic mediated health outcomes. Based on this information, we propose economic and logistical considerations for bringing probiotic therapies to market including regulatory roadblocks, future innovations, and the significant gaps in knowledge requiring additional research to ensure probiotics are suitable long-term options for livestock producers as an antibiotic alternative therapy.

Frontiers in Antibiotics

Growth and behavior of North American microbes on Phragmites australis leaves

Phragmites australis subsp. australis is a cosmopolitan wetland grass that is invasive in many regions of the world, including North America, where it co-occurs with the closely related Phragmites australis subsp. americanus. Because the difference in invasive behavior is unlikely to be related to physiological differences, we hypothesize that interactions with unique members of their microbiomes may significantly affect the behavior of each subspecies. Therefore, we systematically inoculated both plant lineages with a diverse array of 162 fungal and bacterial isolates to determine which could (1) differentiate between Phragmites hosts, (2) infect leaves at various stages of development, or (3) obtain plant-based carbon saprophytically. We found that many of the microbes isolated from Phragmites leaves behave as saprophytes. Only 1% (two taxa) were determined to be strong pathogens, 12% (20 taxa) were weakly pathogenic, and the remaining 87% were nonpathogenic. None of the isolates clearly discriminated between host plant lineages, and the Phragmites cuticle was shown to be a strong nonspecific barrier to infection. These results largely agree with the broad body of literature on leaf-associated phyllosphere microbes in Phragmites.

Microorganisms

Subsurface hydrocarbon degradation strategies in low- and high-sulfate coal seam communities identified with activity-based metagenomics

Environmentally relevant metagenomes and BONCAT-FACS derived translationally active metagenomes from Powder River Basin coal seams were investigated to elucidate potential genes and functional groups involved in hydrocarbon degradation to methane in coal seams with high- and low-sulfate levels. An advanced subsurface environmental sampler allowed the establishment of coal-associated microbial communities under in situ conditions for metagenomic analyses from environmental and translationally active populations. Metagenomic sequencing demonstrated that biosurfactants, aerobic dioxygenases, and anaerobic phenol degradation pathways were present in active populations across the sampled coal seams. In particular, results suggested the importance of anaerobic degradation pathways under high-sulfate conditions with an emphasis on fumarate addition. Under low-sulfate conditions, a mixture of both aerobic and anaerobic pathways was observed but with a predominance of aerobic dioxygenases. The putative low-molecular-weight biosurfactant, lichysein, appeared to play a more important role compared to rhamnolipids. The methods used in this study—subsurface environmental samplers in combination with metagenomic sequencing of both total and translationally active metagenomes—offer a deeper and environmentally relevant perspective on community genetic potential from coal seams poised at different redox conditions broadening the understanding of degradation strategies for subsurface carbon.

npj Biofilms and Microbiomes

Active virus-host interactions at sub-freezing temperatures in Arctic peat soil

Background Winter carbon loss in northern ecosystems is estimated to be greater than the average growing season carbon uptake and is primarily driven by microbial decomposers. Viruses modulate microbial carbon cycling via induced mortality and metabolic controls, but it is unknown whether viruses are active under winter conditions (anoxic and sub-freezing temperatures). Results We used stable isotope probing (SIP) targeted metagenomics to reveal the genomic potential of active soil microbial populations under simulated winter conditions, with an emphasis on viruses and virus-host dynamics. Arctic peat soils from the Bonanza Creek Long-Term Ecological Research site in Alaska were incubated under sub-freezing anoxic conditions with H 2 18 O or natural abundance water for 184 and 370 days. We sequenced 23 SIP-metagenomes and measured carbon dioxide (CO 2 ) efflux throughout the experiment. We identified 46 bacterial populations (spanning 9 phyla) and 243 viral populations that actively took up 18 O in soil and respired CO 2 throughout the incubation. Active bacterial populations represented only a small portion of the detected microbial community and were capable of fermentation and organic matter degradation. In contrast, active viral populations represented a large portion of the detected viral community and one third were linked to active bacterial populations. We identified 86 auxiliary metabolic genes and other environmentally relevant genes. The majority of these genes were carried by active viral populations and had diverse functions such as carbon utilization and scavenging that could provide their host with a fitness advantage for utilizing much-needed carbon sources or acquiring essential nutrients. Conclusions Overall, there was a stark difference in the identity and function of the active bacterial and viral community compared to the unlabeled community that would have been overlooked with a non-targeted standard metagenomic analysis. Our results illustrate that substantial active virus-host interactions occur in sub-freezing anoxic conditions and highlight viruses as a major community-structuring agent that likely modulates carbon loss in peat soils during winter, which may be pivotal for understanding the future fate of arctic soils' vast carbon stocks.

Microbiome

Cotton farming affects ileal virome in a sedentary wild passerine

Although a few studies have focused on avian gut virome variation in response to environmental stressors, none have assessed virome in relation to the production of chemically intensive crop-based agriculture that alters food resources and detrimentally affects various aspects of avian health and fitness. In this study, we used shotgun metatranscriptomics to assess whether exposure to cotton ( Gossypium spp.) production had a deleterious effect on the ileal virome of sedentary northern mockingbirds ( Mimus polyglottos ) sampled from two cotton-producing areas (16 birds in total) and one uncultivated area (7 birds) in Texas, USA. We recovered 43 viruses representing 13 virus families, which included two viruses that appear to be potential vertebrate pathogens. Individual sample richness varied from 25 to 33 viruses. Both virome richness (Adj. r 2 = 0.247, F (2, 20) = 4.615, P = 0.022) and composition (r 2 = 0.370, F (2, 20) = 5.883, P = 0.001) differed among three sampling regions. Cotton production was associated with the increase of virome richness (Adj. r 2 = 0.283, df = 22, P = 0.005). Pesticide occurrence data collected using silicone bands at the three sites suggest that virome compositional changes are not only associated with total pesticide exposure but are also particularly sensitive to the pesticide combinations detected at each location.

Texas