An official website of the United States government
ABSTRACT Microbial communities play critical roles in ecosystem functioning across a wide range of environmental conditions. The physiological stress imposed by temperature, pH and resource levels can shape the structure and function of microbial communities; however, while often tested independently, factors influencing physiological stress on a community rarely occur in isolation from each other. Controlled experiments simultaneously testing multiple interactive stressors allow researchers to better assess the dynamical responses of microbial communities to rapidly changing environments. Using a full factorial, controlled experiment, we tested three hypotheses for how independent and interactive effects of abiotic stresses impact bacterial community composition, structure and function in a model system. We utilised an aquatic, pitcher plant‐associated bacterial community in which microbial nutrient cycling is essential to the host plant and ecosystem. Temperature, pH and resource (food) concentration had strong independent and interactive effects on bacterial community composition, structure and function. Community functions did not respond to interactive stressors in the same way. Chitinase and protease enzymatic activities had opposite responses to temperature and pH changes, indicating that diverse functional measures are necessary for understanding the varied effects of interacting stressors. The most extreme abiotic stress combination (high temperature, lowest pH and excess food) resulted in the lowest enzyme activity and reduced species richness as compared to the other treatments. Stressful conditions, especially high temperature, strengthened correlations between community structure and function. Higher phylogenetic dispersion under abiotic extremes suggested selection for diverse taxa adapted to similar conditions through convergent evolution. These interactive effects highlight the often greater‐than‐additive impact of multiple stressors and demonstrate that environmental filtering and trait convergence shape microbial responses to stress.
more »
« less
Single-strain behavior predicts responses to environmental pH and osmolality in the gut microbiota
To achieve greater predictability in microbiota studies, it is crucial to consider physical environmental factors such as pH and particle concentration, as they play a pivotal role in influencing bacterial function and survival. For example, pH is significantly altered in various diseases, including cancers, inflammatory bowel disease, as well in the case of over-the-counter drug use. Additionally, conditions like malabsorption can affect particle concentration. In our study, we investigate how changes in environmental pH and osmolality can serve as predictive indicators of bacterial growth and abundance. Our research provides a comprehensive resource for anticipating shifts in microbial composition and gene abundance during complex perturbations. Moreover, our findings underscore the significance of the physical environment as a major driver of bacterial composition. Finally, this work emphasizes the necessity of incorporating physical measurements into animal and clinical studies to better understand the factors influencing shifts in microbiota abundance.
more »
« less
- Award ID(s):
- 2109890
- PAR ID:
- 10458377
- Editor(s):
- Blaser, Martin J.
- Date Published:
- Journal Name:
- mBio
- ISSN:
- 2150-7511
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Host‐associated microbiota can be affected by factors related to environmental change, such as urbanization and invasive species. For example, urban areas often affect food availability for animals, which can change their gut microbiota. Invasive parasites can also influence microbiota through competition or indirectly through a change in the host immune response. These interacting factors can have complex effects on host fitness, but few studies have disentangled the relationship between urbanization and parasitism on an organism's gut microbiota. To address this gap in knowledge, we investigated the effects of urbanization and parasitism by the invasive avian vampire fly (Philornis downsi) on the gut microbiota of nestling small ground finches (Geospiza fuliginosa) on San Cristóbal Island, Galápagos. We conducted a factorial study in which we experimentally manipulated parasite presence in an urban and nonurban area. Faeces were then collected from nestlings to characterize the gut microbiota (i.e. bacterial diversity and community composition). Although we did not find an interactive effect of urbanization and parasitism on the microbiota, we did find main effects of each variable. We found that urban nestlings had lower bacterial diversity and different relative abundances of taxa compared to nonurban nestlings, which could be mediated by introduction of the microbiota of the food items or changes in host physiology. Additionally, parasitized nestlings had lower bacterial richness than nonparasitized nestlings, which could be mediated by a change in the immune system. Overall, this study advances our understanding of the complex effects of anthropogenic stressors on the gut microbiota of birds.more » « less
-
To understand how microbiota influence plant populations in nature, it is important to examine the biogeographic distribution of plant-associated microbiomes and the underlying mechanisms. However, we currently lack a fundamental understanding of the biogeography of plant microbiomes across populations and the environmental and host genetic factors that shape their distribution. Leveraging the broad distribution and extensive genetic variation in duckweeds (the Lemna species complex), we identified key factors that governed plant microbiome diversity and compositional variation geographically. In line with the microbial biogeography of free-living microbiomes, we observed higher bacterial richness in temperate regions relative to lower latitudes in duckweed microbiomes (with 10% higher in temperate populations). Our analyses revealed that higher temperature and sodium concentration in aquatic environments showed a negative impact on duckweed bacterial richness, whereas temperature, precipitation, pH, and concentrations of phosphorus and calcium, along with duckweed genetic variation, influenced the biogeographic variation of duckweed bacterial community composition. Analyses of plant microbiome assembly processes further revealed that niche-based selection played an important role (26%) in driving the biogeographic variation of duckweed bacterial communities, alongside the contributions of dispersal limitation (33%) and drift (39%). These findings add significantly to our understanding of host-associated microbial biogeography and provide important insights for predicting plant microbiome vulnerability and resilience under changing climates and intensifying anthropogenic activities.more » « less
-
Abstract Animals generally benefit from their gastrointestinal microbiome, but the factors that influence the composition and dynamics of their microbiota remain poorly understood. Studies of nonmodel host species can illuminate how microbiota and their hosts interact in natural environments. We investigated the role of migratory behaviour in shaping the gut microbiota of free‐ranging barn swallows (Hirundo rustica) by studying co‐occurring migrant and resident subspecies sampled during the autumn migration at a migratory bottleneck. We found that within‐host microbial richness (α‐diversity) was similar between migrant and resident microbial communities. In contrast, we found that microbial communities (β‐diversity) were significantly different between groups regarding both microbes present and their relative abundances. Compositional differences were found for 36 bacterial genera, with 27 exhibiting greater abundance in migrants and nine exhibiting greater abundance in residents. There was heightened abundance ofMycoplasmaspp. andCorynebacteriumspp. in migrants, a pattern shared by other studies of migratory species. Screens for key regional pathogens revealed that neither residents nor migrants carried avian influenza viruses and Newcastle disease virus, suggesting that the status of these diseases did not underlie observed differences in microbiome composition. Furthermore, the prevalence and abundance ofSalmonellaspp., as determined from microbiome data and cultural assays, were both low and similar across the groups. Overall, our results indicate that microbial composition differs between migratory and resident barn swallows, even when they are conspecific and sympatrically occurring. Differences in host origins (breeding sites) may result in microbial community divergence, and varied behaviours throughout the annual cycle (e.g., migration) could further differentiate compositional structure as it relates to functional needs.more » « less
-
Abstract BackgroundSpecies host diverse microbial communities that can impact their digestion and health, which has led to much interest in understanding the factors that influence their microbiota. We studied the developmental, environmental, and social factors that influence the microbiota of nestling barn owls (Tyto alba) through a partial cross-fostering experiment that manipulated the social and nest environment of the nestlings. We then examined the nestling microbiota before and three weeks after the exchange of nestlings between nests, along with the microbiota of the adults at the nest and nestlings in unmanipulated nests. ResultsWe found that nestlings had higher bacterial diversity and different bacterial communities than adults. The microbiota of nestlings was more like that of their mothers than their fathers, but the similarity to the father tended to increase with the amount of time the father was in close proximity to the nest, as measured from movement data. Cross-fostered offspring had higher bacterial diversity and greater changes in bacterial community composition over time than control offspring. Cross-fostering led the microbiota of the nestlings in the experiment to converge on similar bacterial communities. The microbiota of nestling owls therefore rapidly changed along with alterations to their social and nest environments. ConclusionsThese results highlight the dynamic nature of the microbiota during early development and that social interactions can shape microbial communities.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/mbio.00753-23
