Search bioRxiv⌕ Search

Biology subjects

Bohannan, B. J. M.

Publications and source records attributed to Bohannan, B. J. M..

16 recordsLinked to original sources

Fungal:bacterial biomass balance links environmental gradients to soil respiration across a forest-to-marsh transition

Soil microbes regulate whether carbon is retained in soils or returned to the atmosphere through respiration, but the extent to which microbial community characteristics improve the prediction of heterotrophic soil CO2 production beyond predictions by environmental controls remains unclear. We tested this across a topographically structured forest-to-marsh gradient in coastal Oregon by measuring heterotrophic soil respiration, soil physicochemical properties, PLFA-based microbial biomass, metagenomic taxonomic composition, and functional gene-based trait indicators. Across the gradient, soil moisture increased from forest to marsh, while mineral soil and organic matter C:N decreased. These environmental shifts were accompanied by strong but uneven microbial responses: total microbial, fungal, and bacterial biomass declined from forest to marsh, taxonomic composition showed the strongest structuring by environmental conditions, and functional gene-based indicators showed mixed relationships with the gradient. Environmental model comparisons identified soil moisture and organic layer C as the strongest baseline predictors of respiration. Among microbial descriptors, only a small subset improved respiration prediction beyond this environmental baseline. The fungal:bacterial (F:B) biomass ratio produced the largest increase in model fit and the greatest reduction in AICc, whereas the best taxonomic and functional-gene predictors yielded more minor gains. Our results showed that the microbial descriptors most responsive to environmental gradients were not the ones most useful for predicting soil respiration; instead, a relatively simple biomass-partitioning metric captured respiration-relevant microbial variation more effectively than finer taxonomic and genomic descriptors. This suggests that F:B ratio may be especially useful for representing respiration-relevant microbial variation in local landscape-scale studies and for future carbon cycle models applied across heterogeneous ecosystem transition zones.

ecology↗

Predatory bacteria impact C. elegans life-history traits by modulating microbiota community dynamics and thereby vitamin B12 availability

Predatory bacteria such as Bdellovibrio are emerging as ecological modulators in microbial communities by restructuring community composition, yet their roles in host-associated microbiomes remain poorly understood. Using Caenorhabditis elegans as model host and its defined microbiota, we investigated how two Bdellovibrio strains with distinct prey ranges (B. tiberii MYbb2 and B. krueschi MYbb4) affect microbial community composition and host life-history traits. Both strains consistently altered microbiome composition, with MYbb4 causing more pronounced alpha-diversity shifts and MYbb2 selectively enriching strains of the genus Ochrobactrum which coincided with higher host median lifespan. Genome-based predictions indicate that de novo vitamin B12 synthesis by Ochrobactrum underlies the observed host phenotype, which was confirmed through quantitative measurements of the vitamin in mono-cell cultures. Employing the acdh-1p::GFP transcriptional reporter strain, we confirmed that a diet of B12-producing bacteria suppresses the B12-independent propionate detoxification pathway in the host, demonstrating that bacterially produced B12 is bioavailable to C. elegans. Exogenous B12 supplementation assays further confirmed the lifespan-extending effect. Together, these results suggest that predation-driven enrichment of B12-producing bacteria maintains B12 levels sufficient to detoxify propionyl-CoA via the B12-dependent pathway, preventing the accumulation of toxic metabolic byproducts that would otherwise arise under B12-limiting conditions and reduce host lifespan. Our findings demonstrate that predatory bacteria are important drivers of microbiome structure with direct consequences for host physiology, representing an underappreciated ecological mechanism for microbiome modulation.

ecology↗

Drivers of Variation of the Zebrafish Egg Microbiome

Microbiomes are integral to the fitness of many animals, yet little is known about early-life microbiome assembly. What is known largely comes from studies in non-model organisms, where it is difficult to distinguish host genetics from the environment as drivers of microbiome assembly. Here, we used a popular vertebrate model, zebrafish (Danio rerio), to address the major drivers of environmental assembly in 124 individuals. We surveyed the egg microbiome from fertilization to hatching using 16S rRNA gene sequencing and investigated development stage and parentage as potential drivers of microbiome variation. Phylogenetic diversity of the egg microbiome decreased during development, suggesting that environmental filtering may be a major driver of community assembly. Parentage also had an influence on microbiome assembly; eggs derived from the same clutch were often more similar in microbiome composition compared to eggs derived from different clutches. The effect of parentage on microbiome similarity decreased over development, suggesting that parents may be an initial source of egg microbiome members. The egg microbiome undergoes dramatic compositional shifts during development. Understanding the drivers of this variation is important to consider, especially given the role of the microbiome in health and development, and that early exposure to microbes may shape later animal development. Our findings suggest that parents may serve as an important source of microbial symbionts to their offspring, even in an animal that does not provide parental care, such as laboratory zebrafish, and that the developing egg may play an increasingly important role in driving microbiome variation across individuals. ImportanceEarly-life microbiome composition is integral for establishing the normal functioning of multiple host systems, including the nervous system, gastro-intestinal tract, and immune system. However, the drivers of variation in early-life microbiome composition are underexplored, especially in Danio rerio (zebrafish), an important model organism that has allowed extensive exploration of the role of the microbiome in host health and development. Here, we characterize the microbiome of individual zebrafish eggs and determine the effects of parental identity and developmental time on shaping the egg microbiome prior to hatching. Both parentage and age influence microbiome composition and diversity. We found evidence that species-sorting (i.e. selection of microbes by the egg) is an important driver of microbiome assembly during egg development. Furthermore, the effect of parentage on the microbiome, while significant throughout embryonic development, decays over time. Despite the lack of parental care in laboratory reared zebrafish, these findings suggest that the parents are significant source of microbes to their offspring.

microbiology↗

Assembly of skin microbiomes is more neutral than gut microbiomes in multiple animal species

The gut and external tissues of most animals are colonized by communities of microorganisms that can influence the health, development, and fitness of the host. The composition of these communities can vary greatly between individuals within a host species, and both selective factors (e.g. host immune response) and neutral processes (e.g. random loss of microbial cells) have been shown to contribute to this variation. While it is known that microbiome composition differs between tissues within an individual host, less is known about the ecological processes that underline these differences. To address this, we investigated whether the contribution of neutral ecological processes to microbiome assembly differs between external (skin and scale) and internal (gut) host tissues for a diverse panel of animal hosts. To do this, we fit a neutral ecological model to microbial communities from external and internal tissues across a variety of animal hosts. Strikingly, we discovered that the neutral model was equally or better fit to skin or scale microbial communities across all hosts, suggesting that neutral processes play a larger role in the assembly of skin or scale microbiomes compared to gut microbiomes. Furthermore, we observed that this trend is robust to different definitions of the metacommunity (i.e. the microbial taxa available to colonize a host). Finally, we leveraged a simulation framework to compare the model fits of empirical vs simulated microbial communities. We found that neutral model fits to empirical communities can differ from simulated communities, emphasizing the importance of temporal sampling in profiling animal microbiomes.

ecology↗

Comparative analysis of novel Pseudobdellovibrionaceae genera and species yields insights into the genomics and evolution of bacterial predation mode

Bacteria of the family Pseudobdellovibrionaceae belong to a group of bacteria that kill and feed on other bacteria. The diversity of predation strategies, habitats, and genome characteristics of these bacteria are largely unexplored, despite their ecological and evolutionary importance in microbial communities. Therefore, we characterized new Pseudobdellovibrionaceae strains isolated from the direct environments of three animal hosts: the zebrafish (Danio rerio), the threespine stickleback fish (Gasterosteus aculeatus), and the nematode Caenorhabditis elegans. We used transmission electron microscopy (TEM) and genomic analyses to characterize the morphology and predation modes of our isolates. While most of our isolates exhibited periplasmic (i.e. endoparasitic) predation, one isolate clearly exhibited epibiotic (i.e. exoparasitic) predation and represents only the third confirmed epibiotic strain within its clade. Of our isolates, six are members of five new species in the genus Bdellovibrio and two strains likely represent new genera within the family Pseudobdellovibrionaceae. From metabarcoding data, we found indications that Pseudobdellovibrionaceae are widespread among our three animal hosts. Genomic analyses showed that epibiotic predators lack genes involved in host independence (i.e. prey-independent feeding) and peptidoglycan modification. However, genes unique to epibiotic predators may underlie this predation mode, particularly those involved in cell wall remodeling and recycling. With robust phylogenomic analyses, we show that our novel isolates cluster with previously described Pseudobdellovibrionaceae isolates according to predation mode. Further, by placing Pseudobdellovibrionaceae predators within a wider evolutionary history including other predatory and non-predatory bacteria, we postulate periplasmic predation as the ancestral mode, with more derived epibiotic predators exhibiting genome streamlining.

genomics↗

Quantitative Genetics of Microbiome Mediated Traits

Multicellular organisms host a rich assemblage of associated microorganisms, collectively known as their "microbiomes". Microbiomes have the capacity to influence their hosts fitnesses, but the conditions under which such influences contribute to evolution are not clear. This is due in part to a lack of a comprehensive theoretical framework for describing the combined effects of host and associated microbes on phenotypic variation. Here we address this gap by extending the foundations of quantitative genetic theory to include host-associated microbes, as well as alleles of hosts, as factors that explain quantitative host trait variation. We introduce a way to partition host-associated microbiomes into components relevant for predicting a microbiome-mediated response to selection. We then apply our general framework to a simulation model of microbiome inheritance to illustrate principles for predicting host trait dynamics, and to generalize classical narrow and broad sense heritabilities to account for microbial effects. We demonstrate that microbiome-mediated responses to host-level selection can arise from various transmission modes, not solely vertical, but that the contribution of non-vertical modes can depend strongly on host life history. Our work lays a foundation for integrating microbiome-mediated host variation and adaptation into our understanding of natural variation.

evolutionary biology↗

The Evolution of Microbiome-Mediated Traits

The role of host-associated microbiomes in shaping host fitness is becoming increasingly recognized, and may have important evolutionary consequences. The degree to which microbiomes contribute to host evolution depends on how they are inherited. To understand the conditions under which host evolution is mediated by microbiome inheritance, we introduce a simple mathematical model. Our model tracks the evolution of a quantitative host trait that is mediated by host genotype and host microbiome. Unlike host genotype, the host microbiome may have several routes of transmission, including social contact and environmental acquisition. Our model takes a breeding-value approach to formally generalize classical quantitative genetic theory to account for these various modes of microbiome inheritance. A key prediction of our model is that, as long as microbiomes are transmitted between host generations, their mode of transmission has no effect on host trait dynamics. To understand the conditions required for this result, we analyze microbiome-explicit simulations that break important model assumptions. We then discuss avenues to generalize our model and connections with related concepts. Taken together, this work provides novel insights into the dynamics of non-Mendelian populations, and makes first steps towards establishing a theory of microbiome-mediated trait evolution.

evolutionary biology↗

Response of soil microbiome composition to selection on methane oxidation rate

Microbiomes mediate important ecosystem functions, yet it has proven difficult to determine the relationship between microbiome composition and the rate of ecosystem functions. This challenge remains because it is difficult to manipulate microbiome composition directly, we often cannot know a priori which microbiome members influence the rate of an ecosystem function, and microbiomes can covary strongly with other drivers of ecosystem function, such as the environment. To address these challenges, we imposed artificial selection on whole soil ecosystems over multiple generations to select for microbial communities with a high rate of CH4 oxidation. This approach is potentially powerful because it is biologically "agnostic" in that it makes few assumptions about which taxa are important to function, and repeated passaging with fresh substrate weakens the covariance between microbes and the environment. As a response to selection, we observed a 50.7% increase in CH4 oxidation rate per passage relative to a control that experienced random selection. We estimated that 31.5% of the variation in CH4 oxidation rate in these soils can be attributed to microbiome variation (though this was not significant). We also found that selection did not enrich for known CH4 oxidizers; instead, 12 families not known to oxidize CH4, including Fimbriimonadaceae, Cytophagaceae, and Diplorickettsiaceae, were enriched by selection. This result is in contrast to the typical assumption that the rate of an ecosystem function is limited by the final step in the associated microbial pathway. Our study demonstrates that variation in microbiome composition can contribute to variation in the rate of ecosystem function independent of the environment and that this may not always be limited by the final step in a pathway. This suggests that manipulating microbiome composition directly without altering the environment could be a viable strategy for managing ecosystem functions.

ecology↗

Host and microbiome jointly contribute to adaptation to a complex environment

Most animals and plants have associated microorganisms, collectively referred to as their microbiomes, which can provide essential functions. Given their importance, host-associated microbiomes have the potential to contribute substantially to adaptation of the host-microbiome assemblage (the "metaorganism"). Microbiomes may be especially important for rapid adaptation to novel environments because microbiomes can change more rapidly than host genomes. However, it is not well understood how hosts and microbiomes jointly contribute to metaorganism adaptation. We developed a model system with which to disentangle the contributions of hosts and microbiomes to metaorganism adaptation. We established replicate mesocosms containing the nematode Caenorhabditis elegans co-cultured with microorganisms in a novel complex environment (laboratory compost). After approximately 30 nematode generations (100 days), we harvested worm populations and associated microbiomes, and subjected them to a common garden experiment designed to unravel the impacts of microbiome composition and host genetics on metaorganism adaptation. We observed that adaptation took different trajectories in different mesocosm replicates, with some increasing in fitness and others decreasing, and that interactions between host and microbiome played an important role in these contrasting evolutionary paths. We chose two exemplary mesocosms (one with a fitness increase and one with a decrease) for detailed study. For each example, we identified specific changes in both microbiome composition (for both bacteria and fungi) and nematode gene expression associated with each change in fitness. Our study provides experimental evidence that adaptation to a novel environment can be jointly influenced by host and microbiome.

evolutionary biology↗

Seasonal dynamics of methane cycling microbial communities in Amazonian floodplain sediments.

The Amazonian floodplain forests are dynamic ecosystems of great importance for the regional hydrological and biogeochemical cycles and provide a significant contribution to the global carbon balance. Unique geochemical factors may drive the microbial community composition and, consequently, affect CH4 emissions across floodplain areas. Here we provide the first report of the in situ seasonal dynamics of CH4 cycling microbial communities in Amazonian floodplains. We asked how abiotic factors may affect both overall and CH4 cycling microbial communities and further investigated their responses to seasonal changes. We collected sediment samples during wet and dry seasons from three different types of floodplain forests, along with upland forest soil samples, from the Eastern Amazon, Brazil. We used high-resolution sequencing of archaeal and bacterial 16S rRNA genes combined with real-time PCR to quantify Archaea and Bacteria, as well as key functional genes indicative of the methanogenic (methyl coenzyme-M reductase - mcrA) and methanotrophic (particulate methane monooxygenase - pmoA) metabolisms. Methanogens were found to be present in high abundance in floodplain sediments and they seem to resist to dramatic seasonal environmental changes. Methanotrophs known to use different pathways to oxidise CH4 were detected, including anaerobic archaeal and bacterial taxa, indicating that a wide metabolic diversity may be harboured in this highly variable environment. The floodplain environmental variability, which is affected by the river origin, drives not only the sediment chemistry, but also the composition of the microbial communities. The results presented may contribute to the understanding of the current state of CH4 cycling in this region.

microbiology↗

Phenotypic parallelism during experimental adaptation of a free-living bacterium to the zebrafish gut

Despite the fact that animals encounter a plethora of bacterial species throughout their lives, only a subset are capable of colonizing vertebrate digestive tracts, and these bacteria can profoundly influence the health and development of their animal hosts. However, it is still unknown how bacteria evolve symbioses with animal hosts, and this process is central to both the assembly and function of gut bacterial communities. Therefore, we used experimental evolution to study a free-living bacterium as it adapts to a novel vertebrate host. We serially passaged replicate populations of Shewanella oneidensis, through the digestive tracts of larval zebrafish (Danio rerio). After only 20 passages, representing approximately 200 bacterial generations, isolates from replicate evolved populations displayed an improved ability to colonize larval zebrafish digestive tracts during competition against their unpassaged ancestor. Upon sequencing the genomes of these evolved isolates, we discovered that the two isolates with the highest mean competitive fitness accumulated unique sets of mutations. We characterized the swimming motility and aggregation behavior of these isolates, as these phenotypes have previously been shown to alter host-microbe interactions. Despite exhibiting different biofilm characteristics, both isolates evolved augmented swimming motility. These enhancements are consistent with expectations based on the behavior of a closely related Shewanella strain previously isolated from the zebrafish digestive tract and suggest that our evolved isolates are pursuing a convergent adaptive trajectory with this zebrafish isolate. In addition, parallel enhancements in swimming motility among isolates from independently adapted populations implicates increased dispersal as an important factor in facilitating the onset of host association. Our results demonstrate that free-living bacteria can rapidly improve their associations with vertebrate hosts.

evolutionary biology↗

Belowground changes to community structure alter methane-cycling dynamics in Amazonia

Amazonian rainforest is undergoing increasing rates of deforestation, driven primarily by cattle pasture expansion. Forest-to-pasture conversion has been associated with changes to ecosystem processes, including substantial increases in soil methane (CH4) emission. The drivers of this change in CH4 flux are not well understood. To address this knowledge gap, we measured soil CH4 flux, environmental conditions, and belowground microbial community attributes across a land use change gradient (old growth primary forest, cattle pasture, and secondary forest regrowth) in two Amazon Basin regions. Primary forest soils exhibited CH4 uptake at modest rates, while pasture soils exhibited CH4 emission at high but variable rates. Secondary forest soils exhibited low rates of CH4 uptake, suggesting that forest regrowth following pasture abandonment could reverse the CH4 sink-to-source trend. While few environmental variables were significantly associated with CH4 flux, we identified numerous microbial community attributes in the surface soil that explained substantial variation in CH4 flux with land use change. Among the strongest predictors were the relative abundance and diversity of methanogens, which both increased in pasture relative to forests. We further identified individual taxa that were associated with CH4 fluxes and which collectively explained ~50% of flux variance. These taxa included methanogens and methanotrophs, as well as taxa that may indirectly influence CH4 flux through acetate production, iron reduction, and nitrogen transformations. Each land type had a unique subset of taxa associated with CH4 fluxes, suggesting that land use change alters CH4 cycling through shifts in microbial community composition. Taken together, our results suggest that changes in CH4 flux from agricultural conversion could be driven by microbial responses to land use change in the surface soil, with both direct and indirect effects on CH4 cycling. This demonstrates the central role of microorganisms in mediating ecosystem responses to land use change in the Amazon Basin.

ecology↗

Rainforest-to-pasture conversion stimulates soil methanogenesis across the Brazilian Amazon

The Amazon rainforest is a biodiversity hotspot and large terrestrial carbon sink that is threatened by agricultural conversion. Rainforest-to-pasture conversion leads to the release of a potent greenhouse gas by converting soil from a methane sink into a source. The biotic methane cycle is driven by microorganisms; therefore, this study focused on active methane-cycling microorganisms and their functions across land-use types. We collected intact soil cores from three land use types (primary rainforest, pasture, and secondary rainforest) of two geographically distinct areas of the Brazilian Amazon (Santarem, Para and Ariquemes, Rondonia) and performed DNA stable-isotope probing coupled with metagenomics to identify the active methanotrophs and methanogens. At both locations, we observed a significant change in the composition of the isotope-labeled methane-cycling microbial community across land use types, specifically an increase in the abundance and diversity of active methanogens in pastures. We conclude that a significant increase in the abundance and activity of methanogens in pasture soils could explain the greater methane flux. Furthermore, we found that secondary rainforests recovered as methane sinks, indicating the potential for reforestation to offset greenhouse gas emissions in the tropics. These findings are critical for informing land management practices and global tropical rainforest conservation.

microbiology↗

Community structure ecosystem function relationships in the Congo Basin methane cycle depend on the physiological scale of function

Belowground ecosystem processes can be highly variable and difficult to predict using microbial community data. Here we argue that this stems from at least three issues: 1) complex covariance structure of samples (with environmental conditions or spatial proximity) can make distinguishing biotic drivers a challenge, 2) communities can control ecosystem processes through multiple mechanisms, making the identification of these controls a challenge and 3) ecosystem function assessments can be broad in physiological scale, encapsulating multiple processes with unique microbially mediated controls. We test these assertions using methane (CH4)-cycling processes in soil samples collected along a wetland-to-upland habitat gradient in the Congo Basin. We perform our measurements of function under controlled laboratory conditions and include environmental covariates in statistical analyses to aid in identifying biotic drivers. We divide measurements of microbial communities into four attributes (abundance, activity, composition, and diversity) that represent different forms of community control. Lastly, our process measurements differ in physiological scale, including broader processes (gross methanogenesis and methanotrophy) that involve more mediating groups, to finer processes (hydrogenotrophic methanogenesis and high-affinity CH4 oxidation) with fewer mediating groups. We observed that finer scale processes can be more readily predicted from microbial community structure than broader scale processes. In addition, the nature of those relationships differed, with broad processes limited by abundance while fine-scale processes were associated with diversity and composition. These findings demonstrate the importance of carefully defining the physiological scale of ecosystem function and performing community measurements that represent the range of possible controls on ecosystem processes.

ecology↗

Consistent bacterial responses to land use change across the tropics

Bacterial communities are a major component of global diversity and are intimately involved in most terrestrial biogeochemical processes. Despite their importance, we know far less about the response of bacteria to human-induced environmental change than we do about other organisms. Understanding the response of organisms to land use change is especially pressing for tropical rainforests, which are being altered at a higher rate than any other ecosystem. Here, we conduct a meta-analysis of studies performed in each of the major tropical rainforest regions to ask whether there are consistent responses of belowground bacterial communities to the conversion of tropical rainforest to agriculture. Remarkably, we find common responses despite wide variation across studies in the types of agriculture practiced and the research methodology used to study land use change. These responses include changes in the relative abundance of phyla, most notably decreases in Acidobacteria and Proteobacteria and increases in Actinobacteria, Chloroflexi and Firmicutes. We also find that alpha diversity (at the scale of single soil cores), consistently increases with ecosystem conversion. These consistent responses suggest that, while there is great diversity in agricultural practices across the tropics, common features such as the use of slash-and-burn tactics have the potential to alter bacterial community composition and diversity belowground.

ecology↗

A probabilistic model to identify the core microbial community

The core microbial community has been hypothesized to have essential functions ranging from maintaining health in animals to protection against plant disease. However, the identification of the core microbial community is frequently based on arbitrary thresholds, selecting only the most abundant microorganisms. Here, we developed and tested an approach to identify the core community based on a probabilistic model. The Poisson distribution was used to identify OTUs with a probable occurrence in every sample of a given dataset. We identified the core communities of four extensive microbial datasets, and compared the results with conventional, but arbitrary, methods. The datasets were composed of the microbiomes of humans (tongue, gut, and skin), mice (gut), plant (grapevine) tissue, and the maize rhizosphere. Our proposed method revealed core microbial communities with higher richness and diversity than those previously described. This method also includes a greater number of rare taxa in the core, which are often neglected by arbitrary threshold methods. We demonstrated that our proposed method revels a probable core microbial community for each different habitat, which extend our knowledge about shared microbial communities. Our proposed method may help the next steps proving the essential functions of core microbial communities.\n\nOriginality-Significance StatementMore rigorous and less arbitrary statistical methods could increase knowledge regarding the role of microorganisms and their interactions. Here, we suggest a probabilistic method to identify the microbial core community across systems. Our method identifies a large proportion of the rare community that likely belongs to the microbial core community, which was not identified by conventional methods. Our probabilistic model is a non-arbitrary approach to defining the microbial core community, which may help in the next step of the microbial core community studies.

microbiology↗