Biology subjects

Lennon, J. T.

Publications and source records attributed to Lennon, J. T..

36 records · Page 2Linked to original sources

bioRxiv2021

Evolution of a minimal cell

Possessing only essential genes, a minimal cell can reveal mechanisms and processes that are critical for the persistence and stability of life. Here, we report on how a synthetically constructed minimal cell contends with the forces of evolution compared to a non-minimized cell from which it was derived. Genome streamlining was costly, but 80% of fitness was regained in 2000 generations. Although selection acted upon divergent sets of mutations, the rates of adaptation in the minimal and non-minimal cell were equivalent. The only apparent constraint of minimization involved epistatic interactions that inhibited the evolution of cell size. Together, our findings demonstrate the power of natural selection to rapidly optimize fitness in the simplest autonomous organism, with implications for the evolution of cellular complexity.

evolutionary biology↗

bioRxiv2021

Molecular evolutionary dynamics of energy limited microorganisms

Microorganisms have the unique ability to survive extended periods of time in environments with extremely low levels of exploitable energy. To determine the extent that energy limitation affects microbial evolution, we examined the molecular evolutionary dynamics of a phylogenetically diverse set of taxa over the course of 1,000-days. We found that periodic exposure to energy limitation affected the rate of molecular evolution, the accumulation of genetic diversity, and the rate of extinction. We then determined the degree that energy limitation affected the spectrum of mutations as well as the direction of evolution at the gene level. Our results suggest that the initial depletion of energy altered the direction and rate of molecular evolution within each taxon, though after the initial depletion the rate and direction did not substantially change. However, this consistent pattern became diminished when comparisons were performed across phylogenetically distant taxa, suggesting that while the dynamics of molecular evolution under energy limitation are highly generalizable across the microbial tree of life, the targets of adaptation are specific to a given taxon.

evolutionary biology↗

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↗

bioRxiv2020

Stabilizing role of seed banks and the maintenance of bacterial diversity

Coexisting species often exhibit negative frequency dependence due to mechanisms that promote population growth and persistence when rare. These stabilizing mechanisms can maintain diversity through interspecific niche differences, but also through life-history strategies like dormancy that buffer populations in fluctuating environments. However, there are few tests demonstrating how seed banks contribute to long-term community dynamics and the maintenance of diversity. Using a multi-year, high-frequency time series of bacterial community data from a north temperate lake, we documented patterns consistent with stabilizing coexistence. Bacterial taxa exhibited differential responses to seasonal environmental conditions, while seed bank dynamics helped maintain diversity over winter. Strong negative frequency dependence in rare, but metabolically active, taxa suggested a role for biotic interactions in promoting coexistence. Together, our results provide field-based evidence that niche differences and seed banks contribute to recurring community dynamics and the long-term maintenance of diversity in nature.

ecology↗

bioRxiv2020

Resuscitation of the microbial seed bank alters plant-soil interactions

While microorganisms are recognized for driving belowground processes that influence the productivity and fitness of plant populations, the vast majority of bacteria and fungi in soil belong to a seed bank consisting of dormant individuals. Still, plant performance may be affected by microbial dormancy through its effects on the activity, abundance, and diversity of soil microorganisms. To test how microbial seed banks influence plant-soil interactions, we purified recombinant resuscitation promoting factor (Rpf), a bacterial protein that terminates dormancy. Then, in a factorially designed experiment, we applied the Rpf to soil containing field mustard (Brassica rapa), an agronomically important plant species. Plant biomass was ~33 % lower in the Rpf treatment compared to plants grown with an unmanipulated microbial seed bank. In addition, Rpf reduced soil respiration, decreased bacterial abundance, and increased fungal abundance. These effects of Rpf on plant performance were accompanied by shifts in bacterial community composition, which may have diluted mutualists or resuscitated pathogens. Our findings suggest that changes in microbial seed banks may influence the magnitude and direction of plant-soil feedbacks in ways that affect above- and below-ground biodiversity and function.

ecology↗

bioRxiv2020

Quantifying Parallel Evolution

The degree that the environment determines what genes contribute towards adaptation is a fundamental question in microbial evolution. Microbial populations are often experimentally passaged in different environments and sequenced in order to identify candidates for adaptation in a particular environment. However, there remains the need to develop an appropriate statistical framework to identify genes that acquired more mutations in one environment over the other (i.e., divergent evolution). Here we demonstrate how the evolutionary outcomes among replicate populations in the same environment, known as parallel evolution, can be leveraged to construct an intuitive statistical test for identifying the genes that contribute towards divergent evolution. To accomplish this task, we examined publicly available evolve-and-resequence experiment datasets and found that the distribution of mutation counts among genes can be predicted using an ensemble of independent Poisson random variables. Building on this result, we propose that the degree of divergent evolution at a given gene between populations from two different environments can be modeled as the difference between two Poisson random variables, known as the Skellam distribution. We then propose and apply a statistical test to identify specific genes that contribute towards divergent evolution. IMPORTANCE: There is currently no existing framework that can be leveraged to identify genes that contribute towards divergent evolution in microbial evolution experiments. To correct for this absence, we investigated the distribution of mutation counts among genes in order to identify an appropriate null model. Our observations suggest that divergent evolution within a given gene can be modeled as the difference in the total number of mutations observed between two environments. This quantity is described by a probability distribution known as the Skellam distribution, providing an appropriate statistical test for researchers seeking to identify the set of genes that contribute towards divergent evolution in evolution experiments.

evolutionary biology↗

bioRxiv2020

Microbial community composition is affected by press, but not pulse, seawater intrusion

Tidal freshwater marshes (TFMs) are threatened by seawater intrusion, which can affect microbial communities and alter biogeochemical processes. Here, we report on Seawater Addition Long Term Experiment (SALTEx), a manipulative field experiment that investigated continuous (press) and episodic (pulse, 2 months/yr) inputs of brackish water on microbial communities in a TFM. After 2.5 years, microbial diversity was lower in press treatments than in control (untreated) plots. Sulfate reducers increased in response to both press and pulse treatments whereas methanogens did not differ among treatments. Our results suggest that microbial communities in TFMs are resilient to episodic events, but that continuous seawater intrusion may alter bacterial diversity in ways that affect ecosystem functioning. Scientific Significance StatementSea level rise and seawater intrusion threaten tidal freshwater marshes (TFMs) and the important ecosystem services they provide. Intrusion of seawater in TFMs can occur across a range of timescales, such as episodic events, like storm surges or drought, or continuous intrusion as a result of rising sea level. The effects of these stressors on TFM microbial communities are not well understood. Our multi-year field manipulation of brackish water inputs revealed that microbial communities were resilient to short-term pulses of salinity whereas continuous seawater intrusion led to reduced microbial diversity along with changes in relative abundance of key functional groups. Such alterations may diminish the ability of TFMs to sequester carbon and cycle nutrients.

ecology↗

bioRxiv2020

Microbial community assembly in a multi-layer dendritic metacommunity

A major goal of metacommunity ecology is to infer the local- and regional-scale processes that underlie community assembly. In dendritic ecological networks (e.g., stream metacommunities), branching and directional dispersal connectivity can alter the balance between local and regional factors during assembly. However, the implications of vertical habitat structure (e.g., planktonic versus benthic sediments) in dendritic metacommunities remain unclear. In this study, we analyzed the bacterial metacommunity of a fifth-order mountain stream network to assess habitat differences in the (1) dominant community assembly processes, (2) spatial scaling of community assembly processes, and (3) longitudinal variation in community assembly. Using taxonomic and phylogenetic null modeling approaches, we found habitat-specific spatial patterns of community assembly across the dendritic network. Compositional differences between planktonic and benthic communities were maintained by divergent species sorting, but stochasticity influenced assembly at local scales. Planktonic communities showed scale-dependent assembly, transitioning from convergent sorting at local scales to divergent sorting at regional scales, while sediment community assembly was less scale dependent (convergent sorting remained important across all scales). While divergent sorting structured headwaters in both habitat types, sediment communities converged in structure downstream. Taken together, our results show that vertical habitat structure regulates the scale-dependent processes of community assembly across the dendritic metacommunity.

ecology↗

bioRxiv2019

Low costs of adaptation to dietary restriction

Dietary restriction (DR) is the most successful and widespread means of extending organismal lifespan. However, the evolutionary basis of life extension under DR remains uncertain. The traditional evolutionary explanation is that when organisms experience DR, they allocate endogenous resources to survival and postpone reproduction until conditions improve. However, this life-extension strategy should be maladaptive if DR continues for multiple generations due to tradeoffs between longevity and reproduction. To test this prediction, we subjected the budding yeast Saccharomyces cerevisiae to 1,800 generations of evolution on restricted (i.e., DR) vs. non-restricted diets. Adaptation to a non-restricted diet improved reproductive fitness by 57% on that diet, but provided a much smaller (14%) advantage on a restricted diet. In contrast, adaptation to DR resulted in an approximately 35% increase in reproductive fitness on both restricted and non-restricted diets. Importantly, the life-extending effect of DR did not decrease following long-term evolution on the restricted diet. Thus, contrary to theoretical expectations, we found no evidence that the life-extending DR response became maladaptive during multigenerational DR. Our results suggest the DR response may have a low cost and that this phenomenon may have evolved for reasons that extend beyond the benefits of postponing reproduction.

evolutionary biology↗

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

Dormancy dampens the microbial distance-decay relationship

Much of Earths biodiversity has the capacity to engage in dormancy whereby individuals enter a reversible state of reduced metabolic activity. By increasing resilience to unfavorable conditions, dormancy leads to the accumulation of \"seed banks\" that should diminish the influence of environmental filtering, while allowing passive dispersers to colonize new habitats. Although prevalent among single-celled organisms, evidence that dormancy influences patterns of microbial biodiversity and biogeography is lacking. We constructed geographical and environmental distance-decay relationships (DDRs) using 16S rRNA sequencing to characterize the total (DNA) and the active (RNA) bacterial communities in a regional survey of 49 forested ponds. As expected, the total community harbored greater diversity and exhibited weaker DDRs than the active portion of the community. These empirical observations were robust to different measures of community similarity and random resampling tests. Furthermore, findings from the field survey were reproduced by models that included aspects of dormancy along with the geographical coordinates and environmental characteristics of our study system. In addition to maintaining local diversity, our results support recent theoretical predictions that dormancy shapes geographical patterns of biodiversity.

microbiology↗

bioRxiv2018

Microbial dormancy improves predictability of soil respiration at the seasonal time scale

Climate change is accelerating global soil respiration, which could in turn accelerate climate change. The biological mechanisms through which soil carbon (C) responds to climate are not well understood, limiting our ability to predict future global soil respiration rates. As part of a climate manipulation experiment, we tested whether differences in soil heterotrophic respiration driven by season or climate treatment (RH) are linked to 1) relative abundances of microbes in active and dormant metabolic states, 2) net changes in microbial biomass and/or 3) changes in the relative abundances of microbial groups with different C-use strategies. We used a flow-cytometric single-cell metabolic assay to quantify the abundance of active and dormant microbes, and the phospholipid fatty acid (PLFA) method to determine microbial biomass and ratios of fungi:bacteria and Gram-positive:Gram-negative bacteria. RH did not respond to climate treatments but was greater in the warm and dry summer than in the cool and less-dry fall. These dynamics were better explained when microbial data were taken into account compared to when only physical data (temperature and moisture) were used. Overall, our results suggest that RH responses to temperature are stronger when soil contains more active microbes, and that seasonal patterns of RH can be better explained by shifts in microbial activity than by shifts in the relative abundances of fungi and Gram-positive and Gram-negative bacteria. These findings contribute to our understanding of how and under which conditions microbes influence soil C responses to climate.

microbiology↗

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

Diversity and composition of cave methanotrophic communities

Methane oxidizing microorganisms (methanotrophs) are ubiquitous in the environment and represent a major sink for the greenhouse gas methane (CH4). Recent studies have demonstrated that methanotrophs are abundant and contribute to CH4 dynamics in caves. However, very little is known about what controls the distribution and abundance of methanotrophs in subterranean ecosystems. Here, we report a survey of soils collected from > 20 caves in North America to elucidate the factors shaping cave methanotroph communities. Using 16S rRNA sequencing, we recovered methanotrophs from nearly all (98 %) of the samples, including cave sites where CH4 concentrations were at or below detection limits ([≤] 0.3 ppmv). We identified a core methanotroph community among caves that was comprised of high-affinity methanotrophs. Although associated with local-scale mineralogy, methanotroph composition did not systematically vary between the entrances and interior of caves, where CH4 concentrations varied. We also observed that methanotrophs are able to disperse readily between cave systems showing these organisms have low barriers to dispersal. Last, the relative abundance of methanotrophs was positively correlated with cave-air CH4 concentrations suggesting that these microorganisms contribute to CH4 flux in subterranean ecosystems. IMPORTANCERecent observations have shown that the atmospheric greenhouse gas methane (CH4) is consumed by microorganisms (methanotrophs) in caves at rates comparable to CH4 oxidation in surface soils. Caves are abundant in karst landscapes that comprise 14 % of Earths land surface area, and therefore may represent a potentially important, but overlooked CH4 sink. We sampled cave soils to gain a better understand the community composition and structure of cave methanotrophs. Our results show that the members of the USC-{gamma} clade are dominant in cave communities and can easily disperse through the environment, that methanotroph relative abundance was correlated with local scale mineralogy of soils, and that the relative abundance of methanotrophs was positively correlated with CH4 concentrations in cave air.

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

Nutrient stoichiometry shapes microbial coevolution

Coevolution is a force contributing to the generation and maintenance of biodiversity. It is influenced by environmental conditions including the scarcity of essential resources, which can drive the evolution of defense and virulence traits. We conducted a long-term chemostat experiment where the marine cyanobacterium Synechococcus was challenged with a lytic phage under nitrogen (N) or phosphorus (P) limitation. This manipulation of nutrient stoichiometry altered the stability of host-parasite interactions and the underlying mode of coevolution. By assessing infectivity with >18,000 pairwise challenges, we documented directional selection for increased phage resistance, consistent with arms-race dynamics while phage infectivity fluctuated through time, as expected when coevolution is driven by negative frequency-dependent selection. The resulting infection networks were 50 % less modular under N-versus P-limitation reflecting host-range contraction and asymmetric coevolutionary trajectories. Nutrient stoichiometry affects eco-evolutionary feedbacks in ways that may alter the dynamics and functioning of environmental and host-associated microbial communities.

microbiology↗

bioRxiv2017

Evolution with a seed bank: the population genetic consequences of microbial dormancy

Dormancy is a bet-hedging strategy that allows organisms to persist through conditions that are sub-optimal for growth and reproduction by entering a reversible state of reduced metabolic activity. Dormancy allows a population to maintain a reservoir of genetic and phenotypic diversity (i.e., a seed bank) that can contribute to the long-term survival of a population. This strategy can be potentially adaptive and has long been of interest to ecologists and evolutionary biologists. However, comparatively little is known about how dormancy influences the fundamental evolutionary forces of genetic drift, mutation, selection, recombination, and gene flow. Here, we investigate how seed banks affect the processes underpinning evolution by reviewing existing theory, implementing novel simulations, and determining how and when dormancy can influence evolution as a population genetic process. We extend our analysis to examine how seed banks can alter macroevolutionary processes, including rates of speciation and extinction. Through the lens of population genetic theory, we can understand the extent that seed banks influence microbial evolutionary dynamics.

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↗