Biology subjects

Hogle, S. L.

Publications and source records attributed to Hogle, S. L..

8 recordsLinked to original sources

bioRxiv2025

Evolution induced state shifts in a long-term microbial community experiment

Biological communities are complex, dynamic systems that underpin ecosystem functionality1, yet their long-term dynamics and predictability remain poorly understood2. Understanding how Darwinian evolution shapes these systems through eco-evolutionary feedbacks is a central challenge in ecology and evolution. Experimental studies using simplified microbial assemblages have yielded important insights into the ecological principles governing community states3-5. However, an important knowledge gap is how selection within member species drives changes of community state in multispecies systems. Here, we present a four-year evolution experiment involving a 23-species synthetic bacterial community propagated in two environments: a control medium and the same medium supplemented with the antibiotic streptomycin. Through combined analyses of community composition and genome evolution, we quantified the temporal changes in species abundances and the evolutionary trajectories of individual community members. The extended duration of the experiment enabled the detection of adaptive mutations and community state shifts that occur only over long evolutionary timescales. We show that community dynamics are environment dependent and reproducible across replicates, and that evolution of streptomycin resistance in a previously streptomycin-sensitive species on its own can induce abrupt community state shifts. Our results provide a direct demonstration of eco-evolutionary feedbacks within a multi-species community, revealing how a single adaptive mutation can reorganize complex ecological networks.

ecology↗

bioRxiv2024

Global niche partitioning of purine and pyrimidine cross-feeding among ocean microbes

Cross-feeding involves microbes consuming the exudates of other surrounding microbes, mediating elemental cycling. Characterizing the diversity of cross-feeding pathways in ocean microbes illuminates evolutionary forces driving self-organization of ocean ecosystems. Here, we uncover a purine and pyrimidine cross-feeding network in globally abundant groups. The cyanobacterium Prochlorococcus exudes both compound classes, which metabolic reconstructions suggest follows synchronous daily genome replication. Co-occurring heterotrophs differentiate into purine- and pyrimidine-using generalists, or specialists that use compounds for different purposes. The most abundant heterotroph, SAR11, is a specialist that uses purines as sources of energy, carbon and/or nitrogen, with subgroups differentiating along ocean-scale gradients in the supply of energy and nitrogen, in turn producing putative cryptic nitrogen cycles that link many microbes. Finally, in a SAR11 subgroup that dominates where Prochlorococcus is abundant, adenine additions to cultures inhibit DNA synthesis, poising cells for replication. We argue this subgroup uses inferred daily adenine pulses from Prochlorococcus to synchronize to the daily photosynthate supply from surrounding phytoplankton.

ecology↗

bioRxiv2022

Localized coevolution between microbial predator and prey alters community-wide gene expression and ecosystem function

In dynamic and spatially heterogeneous microbial communities, pairs of locally coevolved species interact between themselves and other species across multiple spatial and temporal scales. We currently do not understand how local pairwise coevolutionary processes scale to influence whole microbial communities and how local coevolutionary processes affect wider species interaction networks. Here we investigate the community-wide functional response to a coevolutionary mismatch between a focal bacterial prey species and its ciliate predator in a synthetic 30 species microbial community over two months. We observed that the coevolved prey had little influence on community structure or carrying capacity in the presence or absence of the coevolved predator. However, community metabolic potential (represented by per-cell ATP concentration) was significantly higher in the presence of both coevolved focal species. This ecosystem-level response was mirrored by community-wide transcriptional shifts that resulted in the differential regulation of nutrient acquisition and surface colonization pathways across multiple species. Our findings suggest that the disruption of localized pairwise coevolution can alter community-wide transcriptional networks, even when the overall ecological response is muted. We propose that these altered expression patterns may be an important signal of future diversification and ecological change. SignificanceClosely interacting microbial species pairs (e.g., predator and prey) can become coadapted via reciprocal natural selection. A fundamental challenge in evolutionary ecology is to untangle how coevolution in small species groups affects and is affected by biotic interactions in diverse communities. We conducted an experiment with an idealized 30 species microbial community where we experimentally manipulated the coevolutionary history of a predator and a single prey species. Altering the coevolutionary history of the prey had little effect on the ecology of the system but induced large functional changes in community transcription and metabolic potential. Our results illustrate that localized coevolutionary processes between species pairs can reverberate through ecosystem-scale transcriptional networks with important consequences for broader ecosystem function.

ecology↗

bioRxiv2021

Siderophores as an iron source for Prochlorococcus in deep chlorophyll maximum layers of the oligotrophic ocean

Prochlorococcus is one of the most abundant photosynthesizing organisms in the oligotrophic oceans. Gene content variation among Prochlorococcus populations in separate ocean basins often mirrors the selective pressures imposed by the regions distinct biogeochemistry. By pairing genomic datasets with trace metal concentrations from across the global ocean, we show that the genomic capacity for siderophore-mediated iron uptake is widespread in low-light adapted Prochlorococcus populations from iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcus siderophore consumers were absent in the N. Atlantic ocean (higher iron flux) but constituted up to half of all Prochlorococcus genomes from metagenomes in the N. Pacific (lower iron flux). Prochlorococcus siderophore consumers, like many other bacteria with this trait, also lack siderophore biosynthesis genes indicating that they scavenge exogenous siderophores from seawater. Statistical modeling suggests that the capacity for siderophore uptake is endemic to remote ocean regions where atmospheric iron fluxes are the smallest, particularly at deep chlorophyll maximum and primary nitrite maximum layers. We argue that abundant siderophore consumers at these two common oceanographic features could be a symptom of wider community iron stress, consistent with prior hypotheses. Our results provide a clear example of iron as a selective force driving the evolution of Prochlorococcus.

ecology↗

bioRxiv2021

Within-species trait diversity reorganizes consumer competitive hierarchy and prey community structure in an experimental microbial ecosystem

A popular idea in ecology is that trait variation among individuals from the same species may promote the coexistence of competing species. However, theoretical and empirical tests of this idea have yielded inconsistent findings. We manipulated intraspecific trait diversity in a ciliate competing with a nematode for bacterial prey in experimental microcosms. We found that intraspecific trait variation inverted the original competitive hierarchy to favor the consumer with variable traits, ultimately resulting in competitive exclusion. This competitive outcome was driven by foraging traits (size, speed, and directionality) that increased the ciliates fitness ratio and niche overlap with the nematode. The interplay between consumer trait variation and competition resulted in non-additive cascading effects - mediated through prey defense traits - on prey community assembly. Our results suggest that predicting consumer competitive population dynamics and the assembly of prey communities will require understanding the complexities of trait variation within consumer species.

ecology↗

bioRxiv2020

Novel integrative elements and genomic plasticity in ocean ecosystems

Horizontal gene transfer accelerates microbial evolution, promoting diversification and adaptation. The globally abundant marine cyanobacterium Prochlorococcus has a highly streamlined genome with frequent gene exchange reflected in its extensive pangenome. The source of its genomic variability, however, remains elusive since most cells lack the common mechanisms that enable horizontal gene transfer, including conjugation, transformation, plasmids and prophages. Examining 623 genomes, we reveal a diverse system of mobile genetic elements - cargo-carrying transposons we named tycheposons - that shape Prochlorococcus genomic plasticity. The excision and integration of tycheposons at seven tRNA genes drive the remodeling of larger genomic islands containing most of Prochlorococcus flexible genes. Most tycheposons carry genes important for niche differentiation through nutrient acquisition; others appear similar to phage parasites. Tycheposons are highly enriched in extracellular vesicles and phage particles in ocean samples, suggesting efficient routes for their dispersal, transmission and propagation. Supported by evidence for similar elements in other marine microbes, our work underpins the role of vesicle- and virus-mediated transfer of mobile genetic elements in the diversification and adaptation of microbes in dilute aquatic environments - adding a significant piece to the puzzle of what governs microbial evolution in the planets largest habitat.

microbiology↗

bioRxiv2020

Phosphonate production by marine microbes: exploring new sources and potential function

Phosphonates, organic compounds with a C-P bond, constitute 20-25% of phosphorus in high molecular weight dissolved organic matter and are a significant phosphorus source for marine microbes. However, little is known about phosphonate sources, biological function, or biogeochemical cycling. Here, we determine the biogeographic distribution and prevalence of phosphonate biosynthesis potential using thousands of genomes and metagenomes from the upper 250 meters of the global ocean. Potential phosphonate producers are taxonomically diverse, occur in widely distributed and abundant marine lineages (including SAR11 and Prochlorococcus) and their abundance increases with depth. Within those lineages, phosphonate biosynthesis and catabolism pathways are mutually exclusive, indicating functional niche partitioning of organic phosphorus cycling in the marine microbiome. Surprisingly, one strain of Prochlorococcus (SB) can allocate more than 40% of its cellular P-quota towards phosphonate production. Chemical analyses and genomic evidence suggest that phosphonates in this strain are incorporated into surface layer glycoproteins that may act to reduce mortality from grazing or viral infection. Although phosphonate production is a low-frequency trait in Prochlorococcus populations (~ 5% of genomes), experimentally derived production rates suggest that Prochlorococcus could produce a significant fraction of the total phosphonate in the oligotrophic surface ocean. These results underscore the global biogeochemical impact of even relatively rare functional traits in abundant groups like Prochlorococcus and SAR11.

biochemistry↗

bioRxiv2018

Co-culture and biogeography of Prochlorococcus and SAR11

Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 x 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew as much as 70% faster in the presence of Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11s central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, likely due to production and release of glycine betaine by MIT9313. Evidence suggests that Prochlorococcus MIT9313 may also compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To place our results in context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 - highlighting the biogeochemical potential of these two groups.

microbiology↗