Biology subjects

Muscarella, M. E.

Publications and source records attributed to Muscarella, M. E..

9 recordsLinked to original sources

bioRxiv2024

Resuscitation-promoting factor (Rpf) terminates dormancy among diverse soil bacteria

Microorganisms often inhabit environments that are suboptimal for growth and reproduction. To survive when challenged by such conditions, individuals may engage in dormancy where they enter a metabolically inactive state. For this persistence strategy to confer an evolutionary advantage, microorganisms must be able to resuscitate and reproduce when conditions improve. Among bacteria in the phylum Actinomycetota, dormancy can be terminated by resuscitation-promoting factor (Rpf), an exoenzyme that hydrolyzes glycosidic bonds in the peptidoglycan of the cell wall. We characterized Rpf from Micrococcus KBS0714, a bacterium isolated from agricultural soil. Compared to previous studies, the Rpf elicited activity at relatively high concentrations, yet demonstrated high substrate affinity. Site-directed mutations at conserved catalytic sites significantly reduced or abolished resuscitation, as did the deletion of repeating motifs in a lectin-encoding linker region. We then tested the effects of recombinant Rpf from Micrococcus KBS0714 on a diverse set of dormant soil bacteria. Patterns of resuscitation mapped onto strain phylogeny, which reflected core features of the cell envelope. Additionally, the direction and magnitude of the Rpf effect were associated with functional traits, in particular, aspects of the moisture niche and biofilm production, which are critical for understanding persistence and resuscitation during dormancy. These findings expand our understanding of how Rpf may affect seed-bank dynamics and have implications for the diversity and functioning of soil ecosystems.

microbiology↗

bioRxiv2021

Bacterial composition reflects fine-scale salinity changes while phylogenetic diversity exhibits a strong salt divide

Climate change induced salinization events are predicted to intensify and lead to increased salt stress in freshwater aquatic ecosystems. As a consequence, formerly distinct abiotic conditions and associated biotic communities merge, and the emergence, loss, and persistence of microbial taxa modify the types and rates of ecosystem processes. This study examined how bacterial taxonomic and phylogenetic diversity and ecosystem function respond to acute salinization events where freshwater and estuarine communities and environments coalesce. We hypothesized that when the salinity change outpaces microbial adaptation or saline microbial populations are not yet established in formerly freshwater conditions, then these aquatic communities will exhibit diminished carbon cycling rates, decreased microbial diversity, and altered composition of microbial communities compared to historically freshwater communities. We used an experimental mesocosm approach to determine how salinity and the merging of distinct communities influenced resultant bacterial community structure and function. Each mesocosm represented different salinities (0, 5, 9, 13 psu). Two dispersal treatments, representing aquatic communities sourced from brackish 13 psu ponds and a mix of 13 psu and freshwater ponds, were added to all salinity levels and replicated four times. Results revealed that salinity, but not dispersal, decreased bacterial taxonomic and phylogenetic diversity. Carbon mineralization rates were highest in freshwater conditions and associated to bacterial taxa represented in low relative abundance. Acute salinity changes, such as localized flooding due to storm surge, will more negatively affect freshwater aquatic communities compared to chronic exposure to salinization where the communities have had time to adapt or turnover. IMPORTANCE STATEMENTClimate change induced salinization results in the mixing of formerly distinct environmental conditions and aquatic communities. This study examined the consequence of short-term, acute salinity stress on aquatic bacterial taxonomic and phylogenetic diversity and ecosystem function using an experimental approach. Results revealed that salinity, but not the source of aquatic communities, decreased bacterial taxonomic and phylogenetic diversity. Carbon mineralization rates, which represented ecosystem function, were highest in freshwater conditions and also associated with indicator bacterial taxa in low abundance relative to the total microbial community. Taken together, acute salinity changes will more negatively affect freshwater aquatic communities compared to chronic exposure to salinization where the communities have had time to adapt or turnover resulting in recovered biogeochemical functions.

ecology↗

bioRxiv2021

Microbial population dynamics and evolutionary outcomes under extreme energy-limitation

As the most abundant and diverse form of life on Earth, microorganisms commonly inhabit energy-limited environments where cellular maintenance and growth is highly constrained. To gain insight into how microorganisms persist under such conditions, we derived demographic parameters from a diverse collection of bacteria by censusing 100 populations in a closed system for 1,000 days. All but one taxon survived prolonged resource scarcity, yielding estimated times-to-extinction ranging over four orders of magnitude from 100 - 105 years. These findings corroborate reports of long-lived bacteria that have been recovered from ancient environmental samples, while providing insight into mechanisms of persistence. Critically, we found that as death rates declined over time, lifespan was extended through the scavenging of dead cells. Although growth and reproduction were dramatically suppressed in the absence of an exogenous resource supply, bacterial populations continued to evolve. Hundreds of mutations were acquired, contributing to genome-wide signatures of negative selection as well as molecular signals of adaptation. Remarkable consistency in the ecological and evolutionary dynamics indicate that distantly related bacteria respond to energy-limitation in a similar and predictable manner, which likely contributes to the stability and robustness of microbial life.

microbiology↗

bioRxiv2019

Metabolic insight into bacterial community assembly across ecosystem boundaries

The movement of organisms across habitat boundaries has important consequences for populations, communities, and ecosystems. However, because most species are not well adapted to all habitat types, dispersal into suboptimal habitats could induce physiological changes associated with persistence strategies that influence community assembly. For example, high rates of cross-boundary dispersal are thought to maintain sink populations of terrestrial bacteria in aquatic habitats, but these bacteria may also persist by lowering their metabolic activity, introducing metabolic heterogeneity that buffers the population against niche selection. To differentiate between these assembly processes, we analyzed bacterial composition along a hydrological flow path from terrestrial soils through an aquatic reservoir by sequencing the active and total (active + inactive) portions of the community. When metabolic heterogeneity was ignored, our data were consistent with views that cross-boundary dispersal is important for structuring aquatic bacterial communities. In contrast, we found evidence for strong niche selection when metabolic heterogeneity was explicitly considered, suggesting that, relative to persistence strategies, dispersal may have a weaker effect on aquatic community assembly than previously thought. By accounting for metabolic heterogeneity in complex communities, our findings clarify the roles of local- and regional-scale assembly processes in terrestrial-aquatic meta-ecosystems.

ecology↗

bioRxiv2019

Species dynamics and interactions via metabolically informed consumer-resource models

Quantifying the strength, sign, and origin of species interactions, along with their dependence on environmental context, is at the heart of prediction and understanding in ecological communities. Pairwise interaction models like Lotka-Volterra provide an important and flexible foundation, but notably absent is an explicit mechanism mediating interactions. Consumer-resource models incorporate mechanism, but describing competitive and mutualistic interactions is more ambiguous. Here, we bridge this gap by modeling a coarse-grained version of a species true, cellular metabolism to describe resource consumption via uptake and conversion into biomass, energy, and byproducts. This approach does not require detailed chemical reaction information, but it provides a more explicit description of underlying mechanisms than pairwise interaction or consumer-resource models. Using a model system, we find that when metabolic reactions require two distinct resources we recover Liebigs Law and multiplicative co-limitation in particular limits of the intracellular reaction rates. In between these limits, we derive a more general phenomenological form for consumer growth rate, and we find corresponding rates of secondary metabolite production, allowing us to model competitive and non-competitive interactions (e.g., facilitation). Using the more general form, we show how secondary metabolite production can support coexistence even when two species compete for a shared resource, and we show how differences in metabolic rates change species abundances in equilibrium. Building on these findings, we make the case for incorporating coarse-grained metabolism to update the phenomenology we use to model species interactions.

ecology↗

bioRxiv2018

Trait-based approach to bacterial growth efficiency

AO_SCPLOWBSTRACTC_SCPLOWBacterial growth efficiency (BGE) is the proportion of assimilated carbon that is converted into biomass and reflects the balance between growth and energetic demands. Often measured as an aggregate property of the community, BGE is highly variable within and across ecosystems. To understand this variation, we first identified how species identity and resource type affect BGE using 20 bacterial isolates belonging to the phylum Proteobacteria that were enriched from north temperate lakes. Using a trait-based approach that incorporated genomic and phenotypic information, we characterized the metabolism of each isolate and tested for predicted trade-offs between growth rate and efficiency. A substantial amount of variation in BGE could be explained at both broad (i.e., order, 20 %) and fine (i.e., strain, 58 %) taxonomic levels. While resource type was a relatively weak predictor across species, it explained > 60 % of the variation in BGE within a given species. Furthermore, a metabolic trade-off (between maximum growth rate and efficiency) and genomic features revealed that BGE is a predictable metabolic feature. Our study suggests that genomic and phylogenetic information may help predict aggregate microbial community functions like BGE and the fate of carbon in ecosystems. OO_SCPLOWRIGINALITYC_SCPLOWO_SCPCAP C_SCPCAPO_SCPLOWANDC_SCPLOW SO_SCPLOWIGNIFICANCEC_SCPLOWBacterial growth efficiency (BGE) is an important yet notoriously variable measure of metabolism that has proven difficult to predict. To better understand how assimilated carbon is allocated, we explored growth efficiency across a collection of bacteria strains using a trait-based approach. Specifically, we measured respiration and biomass formation rates for populations grown in minimal media containing one of three carbon resources. In addition, we collected a suite of physiological traits to describe each strain, and we sequenced the genome of each organism. Our results suggest that species identity and resource type may contribute to growth efficiency when measured as an aggregate property of a natural community. In addition, we identified genomic pathways that are associated with elevated BGE. The findings have implications for integrating microbial metabolism from the cellular to ecosystem scale.

microbiology↗

bioRxiv2018

Resource diversity structures aquatic bacterial communities

Microbial diversity is strongly affected by the bottom-up effects of resource availability. However, because resource pools often exist as heterogeneous mixtures of distinct molecules, resource heterogeneity may also affect community diversity. To test this hypothesis, we surveyed bacterial communities in lakes that varied in resource concentration. In addition, we characterized resource heterogeneity in these lakes using an ecosystem metabolomics approach. Overall, resource concentration and resource heterogeneity affected bacterial resource-diversity relationships. We found strong relationships between bacterial alpha-diversity (richness and evenness) and resource concentration and richness, but richness and evenness responded in different ways. Likewise, we found associations between the composition of the bacterial community and both resource concentration and composition, but the relationship with resource composition was stronger. Last, in the surveyed communities the presence of resource generalists may have reduced the effect of resource heterogeneity on community composition. These results have implications for understanding the interactions between bacteria and organic matter and suggest that changes in organic matter composition may alter the structure and function of bacterial communities.

microbiology↗

bioRxiv2017

Ecological Insights from the Evolutionary History of Microbial Innovations

Bacteria and Archaea represent the base of the evolutionary tree of life and contain the vast majority of phylogenetic and functional diversity. Because these organisms and their traits directly impact ecosystems and human health, a focus on functional traits has become increasingly common in microbial ecology. These trait-based approaches have the potential to link microbial communities and their ecological function. But an open question is how, why, and in what order microorganisms acquired the traits we observe in the present day. To address this, we reconstructed the evolutionary history of microbial traits using genomic data to understand the evolution, selective advantage, and similarity of traits in extant organisms and provide insights into the composition of genomes and communities. We used the geological timeline and physiological expectations to provide independent evidence in support of this evolutionary history. Using this reconstructed evolutionary history, we explored hypotheses related to the composition of genomes. We showed that gene transition rates can be used to make predictions about the size and type of genes in a genome: generalist genomes comprise many evolutionarily labile genes while specialist genomes comprise more highly conserved functional genes. These findings suggest that generalist organisms do not build up and hoard an array of functions, but rather tend to experiment with functions related to environmental sensing, transport, and complex resource degradation. Our results provide a framework for understanding the evolutionary history of extant microorganisms, the origin and maintenanceof traits, and linking evolutionary relatedness and ecological function.

microbiology↗

bioRxiv2017

Relic DNA contributes minimally to estimates of microbial diversity

Extracellular or \"relic\" DNA is one of the largest pools of nucleic acids in the mbiosphere 1,2. Relic DNA can influence a number of important ecological and evolutionary processes, but it may also bias estimates of microbial abundance and diversity, which has implications for understanding environmental, engineered, and host-associated ecosystems. We developed models capturing the fundamental processes that regulate the size and composition of the relic DNA pools to identify scenarios leading to biased estimates of biodiversity. Our models predict that bias increases with relic DNA pool size, but only when the species abundance distributions (SAD) of relic and intact DNA are distinct from one another. We evaluated our model predictions by quantifying relic DNA and assessing its contribution to bacterial diversity using 16S rRNA gene sequences collected from different ecosystem types, including soil, sediment, water, and the mammalian gut. On average, relic DNA made up 33 % of the total bacterial DNA pool, but exceeded 80 % in some samples. Despite its abundance, relic DNA had no effect on estimates of taxonomic and phylogenetic diversity, even in ecosystems where processes such as the physical protection of relic DNA are common and predicted by our models to generate bias. Rather, our findings are consistent with the expectation that relic DNA sequences degrade in proportion to their abundance and therefore may contribute minimally to estimates of microbial diversity.

microbiology↗