Biology subjects

Coe, A.

Publications and source records attributed to Coe, A..

10 recordsLinked to original sources

bioRxiv2026

Defining traits of low-light adapted Prochlorococcus inhabiting surface waters of the Equatorial Pacific Ocean

A diverse array of photosynthetic phytoplankton drives primary production in equatorial surface waters. Among these, the cyanobacterium Prochlorococcus is an important contributor to net primary production in these typically iron-limited, high-nutrient and low-chlorophyll (HNLC) regions. Here, we explore the diversity of these organisms, in part, through targeted enrichment of Prochlorococcus cells using field-based high-speed cell sorting techniques. We demonstrate that the genomes of Prochlorococcus belonging to the low-light adapted LLI clade, and isolated from the surface of the Equatorial Pacific Ocean, are depleted in functions related to the assimilation of urea, nitrite, and amino acids. These are the first examples of LLI Prochlorococcus that have lost the ability to use nitrite, a trait considered to be a core feature of this clade. All new equatorial cultures of LLI Prochlorococcus appear to use a distinct isoform of protoporphyrinogen IX oxidase (HemG), for the biosynthesis of a chlorophyll precursor, that does not require the use of iron-containing heme. In contrast, the heme-dependent HemJ isoform is typically used by Prochlorococcus found outside equatorial HNLC waters. Together, these findings suggest that low-light adapted Prochlorococcus in the equatorial ocean possess accessory gene content that reflects adaptation to the generally iron-limited but nitrogen-replete conditions of surface waters.

microbiology↗

bioRxiv2025

The shared and distinct roles of Prochlorococcus and co-occurring heterotrophic bacteria in regulating community dynamics

Prochlorococcus is the worlds most abundant photosynthetic organism with over 1027 cells distributed across much of Earths oceans, and is collectively responsible for almost 10% of marine carbon fixation. Naturally co-occurring heterotrophic bacteria at roughly 105-106 cells mL-1 in the oceans have been shown to increase Prochlorococcus fitness and productivity. Despite this massive scale, our understanding of these globally important interactions remains limited, with past research largely focused on single Prochlorococcus-heterotroph pairings involving only a few species. In this study, we extend this perspective by using synthetic communities containing multiple diverse heterotrophic strains isolated from Prochlorococcus enrichment cultures. Specifically, we isolated the four most abundant co-occurring heterotroph species and examined both individual Prochlorococcus-heterotroph interactions and interactions within a synthetic community comprising Prochlorococcus and all four heterotrophs. Using absolute quantification of RNA, DNA, and cell counts over the course of Prochlorococcus growth curves, we find that Prochlorococcus has a modest, species-independent transcriptional response to heterotrophs, whereas each heterotroph displays a markedly different transcriptional response to the community and fulfills distinct metabolic roles. Transcriptional analyses reveal several potential crossfeeding interactions and indicate that community dynamics are influenced not only by metabolic activity but also antagonistic mechanisms, defense responses, and coordinated group behaviors. By pairing synthetic community approaches with absolute abundance measurements, we can gain deeper insight into the forces that shape microbial community assembly in the oceans and their role in driving the global carbon cycle.

microbiology↗

bioRxiv2025

Influence of heterotrophs on phage infection of marine picocyanobacteria

Picocyanobacteria Prochlorococcus and Synechococcus coexist with both their lytic phages and heterotrophic bacteria in the oceans. These lytic phages are a significant cause of mortality, and heterotrophic bacteria have been shown to increase the fitness of Prochlorococcus by reducing oxidative stress and cross feeding under extended darkness. Studies of Prochlorococcus-phage interactions are often done with xenic cultures as it has been historically difficult to obtain and maintain heterotroph-free cultures. Here we examine the effects of heterotrophic bacteria on phage infection in Prochlorococcus and Synechococcus by comparing phage infection dynamics in cultures with and without heterotrophs present. We found that Prochlorococcus populations resumed growth following infection only in the presence of heterotrophs, independent of phage:host or heterotroph:host ratios. In phage:host pairing with Synechococcus the outcomes varied, suggesting that the impact of heterotrophs on phage infection may be dependent on the phage:host interaction. In cases where the host recovered from phage infection, heterotrophs appeared to facilitate it both by mitigating oxidative stress and possibly supplying organic carbon sources, which may support post-infection growth. Furthermore, Prochlorococcus and Synechococcus populations that recovered from infection were resistant to phage infection when transferred to fresh media. Evidence argues against genetic change as the mechanism of resistance, suggesting that Prochlorococcus and Synechococcus populations in co-culture with heterotrophs undergo non-genetic adaptations during recovery from phage infection, likely driven by heterotroph-derived organic compounds that reshape host metabolism and confer protection against future lysis.

microbiology↗

bioRxiv2025

ProSynTaxDB: A curated protein database and workflow for taxonomic classification of Prochlorococcus and Synechococcus in metagenomes

Prochlorococcus and Synechococcus are abundant marine picocyanobacteria that contribute significantly to ocean primary production. Recent genome sequencing efforts, including those presented here, have yielded a large number of high-quality reference genomes, enabling the classification of these picocyanobacteria in marine metagenomic sequence data at high phylogenetic resolution. When combined with environmental data, these classifications can guide cluster/clade/grade assignments and offer insights into niche differentiation within these populations. Here we present ProSynTax, a curated protein sequence dataset and accompanying workflow aimed at enhancing the taxonomic resolution of Prochlorococcus and Synechococcus classification. ProSynTax includes proteins from 1,260 genomes of Prochlorococcus and Synechococcus, including single-amplified genomes, high-quality draft genomes, and newly closed genomes. Additionally, ProSynTax incorporates proteins from 41,753 genomes of marine heterotrophic bacteria, archaea, and viruses to assess microbial and viral communities surrounding Prochlorococcus and Synechococcus. This resource enables accurate classification of picocyanobacterial clusters/clades/grades in metagenomic data - even when present at 0.15% of reads for Prochlorococcus or 0.03% of reads for Synechococcus.

bioinformatics↗

bioRxiv2025

Uptake of Prochlorococcus-derived metabolites by Alteromonas macleodii MIT1002 shows high levels of substrate specificity

Seawater contains an abundance of small biomolecules, or metabolites, that are highly labile components of dissolved organic matter (DOM). Marine microbes interact by exchanging metabolites, thus shaping marine microbial ecology, DOM composition, and global carbon cycling. To better constrain one set of microbe-metabolite interactions, we cultured the marine gammaproteobacterium Alteromonas macleodii MIT1002 on a range of compounds excreted by a sympatric cyanobacterium, Prochlorococcus. Alteromonas could assimilate the branched chain amino acids leucine, isoleucine, and valine, as well as 3-methyl-2-oxobutanoic acid (a branched chain ketoacid intermediate of valine metabolism), but not thymidine, kynurenine, 4-hydroxybenzoic acid, or the other branched chain ketoacids. The assimilation of branched chain amino acids indicates that Alteromonas can metabolically process each corresponding ketoacid, suggesting that transporter specificity underlies the observed substrate specificity for 3-methyl-2-oxobutanoic acid. These experiments show that even subtle changes in chemical structure can result in different microbial interactions and different fates for dissolved metabolites. Significance StatementMicrobial interactions with dissolved organic matter are important controls on the marine carbon cycle. Dissolved organic matter is often considered in bulk, which leaves the specificity and nature of these interactions poorly constrained. Here we show that microbe-molecule interactions can be highly specific, distinguishing between molecules that are structurally and biochemically similar. This implies that small changes in this pool of carbon could have large impacts for the overall system function, and that measuring this pool of carbon with molecular-level resolution is important to characterizing microbe-molecule interactions. We further explore the mechanism underlying the observed substrate specificity and suggest that it is caused by transporter selectivity, meaning the ability of these microbes to selectively uptake specific dissolved organic molecules.

microbiology↗

bioRxiv2024

Emergence of metabolic coupling to the heterotroph Alteromonas promotes dark survival in Prochlorococcus

Prochlorococcus is found throughout the euphotic zone in the oligotrophic open ocean. Deep mixing and sinking while attached to particles can, however, transport Prochlorococcus cells below this sunlit zone, depriving them of light for extended periods of time. Previous work has shown that Prochlorococcus by itself cannot survive extended periods of darkness. However, when co-cultured with a heterotrophic microbe and subjected to repeated periods of extended darkness, Prochlorococcus cells develop an epigenetically inherited dark-tolerant phenotype that can survive longer periods of darkness. Here we examine the metabolic and physiological changes underlying this adaptation using co-cultures of dark-tolerant and parental strains of Prochlorococcus, each grown with the heterotroph Alteromonas under diel light:dark conditions. The relative abundance of Alteromonas was higher in dark-tolerant than parental co-cultures, while dark-tolerant Prochlorococcus cells were larger, contained less chlorophyll, and were less synchronized to the light:dark cycle. Meta-transcriptome analysis revealed that dark-tolerant co-cultures undergo a joint change, in which Prochlorococcus undergoes a relative shift from photosynthesis to respiration, while Alteromonas shifts towards using more organic acids instead of sugars. Furthermore, the transcriptome data suggested enhanced biosynthesis of amino acids and purines in dark-tolerant Prochlorococcus and enhanced degradation of these compounds in Alteromonas. Collectively, our results demonstrate that dark adaptation involves a strengthening of the metabolic coupling between Prochlorococcus and Alteromonas, presumably mediated by an enhanced, and compositionally modified, carbon exchange between the two species.

microbiology↗

bioRxiv2023

Novel isolates expand the physiological diversity of Prochlorococcus and illuminate its macroevolution

Prochlorococcus is a diverse picocyanobacterial genus and the most abundant phototroph on Earth. Its photosynthetic diversity divides it into high- or low-light adapted groups representing broad phylogenetic grades - each composed of several monophyletic clades. Here we physiologically characterize four new Prochlorococcus strains isolated from below the deep chlorophyll maximum in the North Pacific Ocean and combine this information with genomic and evolutionary analyses. The isolates belong to deeply-branching low-light adapted clades that have no other cultivated representatives and display some unusual characteristics. For example, despite its otherwise low-light adapted physiological characteristics, strain MIT1223 has low chl b2 content similar to high-light adapted strains. Isolate genomes revealed that each strain contains a unique arsenal of pigment biosynthesis and binding alleles that have been horizontally acquired, contributing to the observed physiological diversity. Comparative genomic analysis of all picocyanobacteria reveals that Pcb, the major pigment carrying protein in Prochlorococcus, greatly increased in copy number and diversity per genome along a branch that coincides with the loss of facultative particle attachment. Collectively, these observations add support to the current macroevolutionary model of picocyanobacteria, where niche constructing radiations allowed ancestral lineages to transition from a particle-attached to planktonic lifestyle and broadly colonize the water column, followed by adaptive radiations near the surface that pushed ancestral lineages deeper in the euphotic zone resulting in modern depth-abundance profiles. Originality-Significance StatementThe marine cyanobacterium, Prochlorococcus, is among the Earths most abundant organisms, and much of its genetic and physiological diversity remains uncharacterized. While field studies help reveal the scope of diversity, cultured isolates allow us to link genomic potential to physiological processes, illuminate eco-evolutionary feedbacks, and test theories arising from comparative genomics of wild cells. Here, we report the isolation and characterization of novel low-light (LL) adapted Prochlorococcus strains that fill in multiple evolutionary gaps. These new strains are the first cultivated representatives of the LLVII and LLVIII paraphyletic grades of Prochlorococcus, which are broadly distributed in the lower regions of the ocean euphotic zone. Each of these grades is a unique, highly diverse section of the Prochlorococcus tree that separates distinct ecological groups: the LLVII grade branches between monophyletic clades that have facultatively particle-associated and constitutively planktonic lifestyles, while the LLVIII grade lies along the branch that leads to all high-light (HL) adapted clades. Characterizing strains and genomes from these grades yields insights into the large-scale evolution of Prochlorococcus. The new LLVII and LLVIII strains are adapted to growth at very low irradiance levels and possess unique light-harvesting gene signatures and pigmentation. The LLVII strains represent the most basal Prochlorococcus group with a major expansion in photosynthetic antenna genes. Further, a strain from the LLVIII grade challenges the paradigm that all LL-adapted Prochlorococcus exhibit high ratios of chl b:a2. These findings provide insights into major transitions in Prochlorococcus evolution, from the benthos to a fully planktonic lifestyle and from growth at low irradiances to the rise of the HL-adapted clades that dominate the modern ocean.

microbiology↗

bioRxiv2022

Environmental and taxonomic drivers of bacterial extracellular vesicle production in marine ecosystems

Extracellular vesicles are small ([~]50-250 nm diameter) membrane-bound structures released by cells into their surrounding environment. Vesicles are abundant in the global oceans and likely play a number of ecological roles in these microbially dominated ecosystems, yet we know nothing about what influences their production and distributions. Here we examine how vesicle production varies among different strains of cultivated marine microbes and explore the degree to which this is influenced by some key environmental variables. We show that vesicle production rates - the number of vesicles produced per cell per generation - vary across an order of magnitude in cultures of marine Proteobacteria, Cyanobacteria, and Bacteroidetes. Vesicle production rates further differ among strains of the cyanobacterium Prochlorococcus, and vary across temperature and light gradients. These data suggest that both community composition and local environmental conditions modulate the production and standing stock of vesicles in the oceans. Examining samples from the oligotrophic North Pacific Gyre, we show depth-dependent changes in the abundance of vesicle-like particles in the upper water column in a manner broadly consistent with culture observations: highest vesicle abundances are found near the surface, where light irradiances and temperatures are greatest, and then decrease with depth. This work represents the beginnings of a quantitative framework for describing extracellular vesicle dynamics in the oceans - essential as we begin to incorporate vesicles into our ecological and biogeochemical understanding of marine ecosystems. ImportanceBacteria secrete extracellular vesicles containing a wide variety of cellular compounds, including lipids, proteins, nucleic acids, and small molecules, into their surrounding environment. These structures are found in diverse microbial habitats, including the oceans, where their distributions vary throughout the water column. Differences in vesicle abundances likely affect their functional impacts within microbial ecosystems, but the factors influencing vesicle distributions in the environment remain poorly understood. Using quantitative analysis of marine microbial cultures, we show that bacterial vesicle production in the oceans is shaped by a combination of biotic and abiotic factors. Our data indicate that different marine taxa release vesicles at rates varying across an order of magnitude, and that vesicle production can change dynamically as a function of environmental conditions. Taken together with direct measurements of vesicle concentrations in the oceans, these culture-based measurements further provide a window into estimating vesicle loss rates. These findings represent a step forward in our understanding of marine vesicle distributions and provide a basis for quantitatively exploring vesicle dynamics in natural ecosystems.

microbiology↗

bioRxiv2020

Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation

The picocyanobacteria Prochlorococcus and Synechococcus are found throughout the oceans euphotic zone, where the daily light:dark cycle drives their physiology. Periodic deep mixing events can, however, move cells below this zone, depriving them of light for extended periods of time. Here we demonstrate that Prochlorococcus and Synechococcus can adapt to tolerate repeated periods of light energy deprivation. Cyanobacterial cultures kept in the dark for 3 days and then returned to the light initially required 18-26 days to resume growth, but after multiple rounds of dark exposure the strains began to regrow after only 1-2 days. This dark-tolerant phenotype was stable and heritable; cultures retained the trait across at least 18-21 generations even when grown in a standard 13:11 light:dark cycle. We found no genetic differences between the dark-tolerant and parental strains of Prochlorococcus NATL2A, indicating that an epigenetic change is responsible for the adaptation. To begin to explore this possibility, we asked whether DNA methylation - an epigenetic mechanism in bacteria - occurs in Prochlorococcus. LC-MS/MS analysis showed that while DNA methylations, including 6mA and 5mC, are found in some other Prochlorococcus strains, no methylations were detected in either the parental or dark-tolerant strain used in our experiments -i.e. the NATL2A strain. These findings suggest that Prochlorococcus utilizes a yet-to-be-determined epigenetic mechanism to adapt to the stress of extended light energy deprivation.

microbiology↗

bioRxiv2020

Microbial Diversity of Co-occurring Heterotrophs in Cultures of Marine Picocyanobacteria

Prochlorococcus and Synechococcus are responsible for around 10% of global net primary productivity, serving as part of the foundation of marine food webs. Heterotrophic bacteria are often co-isolated with these picocyanobacteria in seawater enrichment cultures that contain no added organic carbon; heterotrophs grow on organic carbon supplied by the photolithoautotrophs. We have maintained these cultures of Prochlorococcus and Synechococcus for 100s to 1000s of generations; they represent ideal microcosms for examining the selective pressures shaping autotroph/heterotroph interactions. Here we examine the diversity of heterotrophs in 74 enrichment cultures of these picocyanobacteria obtained from diverse areas of the global oceans. Heterotroph community composition differed between clades and ecotypes of the autotrophic hosts but there was significant overlap in heterotroph community composition. Differences were associated with timing, location, depth, and methods of isolation, suggesting the particular conditions surrounding isolation have a persistent effect on long-term culture composition. The majority of heterotrophs in the cultures are rare in the global ocean; enrichment conditions favor the opportunistic outgrowth of these rare bacteria. We did find a few examples, such as heterotrophs in the family Rhodobacteraceae, that are ubiquitous and abundant in cultures and in the global oceans; their abundance in the wild is also positively correlated with that of picocyanobacteria. Collectively, the cultures converged on similar compositions, likely from bottlenecking and selection that happens during the early stages of enrichment for the picocyanobacteria. We highlight the potential for examining ecologically relevant relationships by identifying patterns of distribution of culture-enriched organisms in the global oceans. IMPORTANCEOne of the biggest challenges in marine microbial ecology is to begin to understand the rules that govern the self-assembly of these complex communities. The picocyanobacteria Prochlorococcus and Synechococcus comprise the most numerous photosynthetic organisms in the sea and supply a significant fraction of the organic carbon that feeds diverse heterotrophic microbes. When initially isolated into cultures, Prochlorococcus and Synechococcus carry with them select heterotrophic microorganisms that depend on them for organic carbon. The cultures self-assemble into stable communities of diverse microorganisms and are microcosms for understanding microbial interdependencies. Primarily faster-growing, relatively rare, copiotrophic heterotrophic bacteria - as opposed to oligotrophic bacteria that are abundant in picocyanobacterial habitats - are selected for in these cultures, suggesting that these copiotrophs experience these cultures as they would high carbon fluxes associated with particles, phycospheres of larger cells, or actual attachment to picocyanobacteria in the wild.

microbiology↗