Biology subjects

Braakman, R.

Publications and source records attributed to Braakman, R..

11 recordsLinked to original sources

bioRxiv2026

Proteomes reflect size-based growth constraints across diverse microbes

The maximum growth rate of microbes plays a central role in shaping ecological outcomes and is a major target of bioengineering efforts. Previous data compilations suggest single cell maximum growth rates mostly decrease with cell volume across species, except for an initial increase from the very smallest microbes to an intermediate size. Here we hypothesized that this unimodal relationship is shaped by the volumetric requirements of ribosomes and the surface area-dependence of nutrient supply. We developed a mechanistic model relating ribosomal protein mass fraction to growth rate and cell size. Predictions from this model were empirically supported by proteomic data from 97 prokaryotes ranging over 3 orders of magnitude in cell volume. Our analysis suggests that the smallest cells' growth rates are restricted by the volumetric constraints on ribosomes per cell and rely on compact, heterotrophic metabolisms. In contrast, growth rates of the largest prokaryotes face geometric constraints on specific resource acquisition rates, capping growth rates and investment in ribosomal protein, but allowing investment in protein-expensive metabolisms including phototrophy and sulfur oxidation. Prokaryotic cells of intermediate size face neither constraint and exhibit a higher maximum growth rate potential, which, we hypothesize, is associated with elevated metabolic diversity.

systems biology↗

bioRxiv2025

Characterization of Phytoplankton-Excreted Metabolites Mediating Carbon Flux through the Surface Ocean

The marine labile dissolved organic carbon (DOC) pool is a dynamic reservoir of thousands of molecules that cycles approximately one-quarter of Earths primary production within days to weeks. After excretion by phytoplankton and other microbes, metabolites are rapidly consumed, resulting in low standing concentrations (picomolar to low nanomolar). Despite the decades-long search for labile DOC sources and molecular identities, marine phytoplankton exometabolomes are not well characterized, largely due to difficulties in measuring small polar molecules in saline water. Here, we profiled the exometabolomes of six axenic phytoplankton species representing key functional groups including a diatom (Thalassiosira pseudonana CCMP1335), a picoeukaryote (Micromonas commoda RCC299), a coccolithophore (Gephyrocapsa huxleyi CCMP371), a diazotrophic cyanobacterium (Crocosphaera watsonii WH8501), and two picocyanobacteria (Prochlorococcus marinus MIT 9301 and Synechococcus WH8102). From these cultures, we quantified 56 amine- and alcohol-containing exometabolites representing 11 compound classes which in sum comprised up to 23.4% of phytoplankton-excreted DOC. We estimated that these phytoplankton-derived exometabolites could supply up to 5% of the daily carbon quota of the dominant heterotrophic bacterium SAR11 in the surface ocean. Substantial variations in exometabolite identity and concentration across phytoplankton taxa underscore taxonomic diversity as a key driver in the supply and composition of labile DOC. This taxonomic variation predicts geographic and seasonal differences in the distribution of marine dissolved metabolites that underpin the cycling of labile DOC back to CO2. Overall, our work suggests that phytoplankton exometabolites are key chemical currencies that mediate significant carbon fluxes within the oceans carbon cycle. Significance StatementPhytoplankton exometabolites are key components of the marine labile dissolved organic carbon (DOC) pool, which drives major a fraction of the oceanic carbon flux. Yet, their composition and flux are poorly constrained. Leveraging new methods, we quantified amine- and alcohol-containing exometabolites in diverse phytoplankton and found they varied taxonomically. These exometabolites accounted for up to 23.4% of excreted DOC, potentially supporting a sizable fraction of the global heterotrophic growth. Integrating our results with ecological models suggest that exometabolite composition varies geographically and seasonally in response to changing phytoplankton community structures. Our findings illuminate the long-standing "black box" of labile DOC and link taxonomic diversity to the chemical currencies underpinning the microbe-metabolite networks at the heart of the marine carbon cycle.

ecology↗

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

Simultaneous acclimation to nitrogen and iron scarcity in open ocean cyanobacteria revealed by sparse tensor decomposition of metatranscriptomes

Microbes respond to changes in their environment by adapting their physiology through coordinated adjustments to the expression levels of functionally related genes. To detect these shifts in situ, we developed a sparse tensor decomposition method that derives gene co-expression patterns from inherently complex whole community RNA-sequencing data. Application of the method to metatranscriptomes of the abundant marine cyanobacteria Prochlorococcus and Synechococcus identified responses to scarcity of two essential nutrients, nitrogen and iron, including increased transporter expression, restructured photosynthesis and carbon metabolism, and mitigation of oxidative stress. Further, expression profiles of the identified gene clusters suggest that both cyanobacteria populations experience simultaneous nitrogen and iron stresses in a transition zone between North Pacific oceanic gyres. The results demonstrate the power of our approach to infer organism responses to environmental pressures, hypothesize functions of uncharacterized genes, and extrapolate ramifications for biogeochemical cycles in a changing ecosystem. TeaserNew analytical approach reveals shifts in gene expression that may help cyanobacteria cope with environmental stressors.

bioinformatics↗

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↗

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↗

bioRxiv2024

Digital Microbe: A Genome-Informed Data Integration Framework for Collaborative Research on Emerging Model Organisms

The remarkable pace of genomic data generation is rapidly transforming our understanding of life at the micron scale. Yet this data stream also creates challenges for team science. A single microbe can have multiple versions of genome architecture, functional gene annotations, and gene identifiers; additionally, the lack of mechanisms for collating and preserving advances in this knowledge raises barriers to community coalescence around shared datasets. "Digital Microbes" are frameworks for interoperable and reproducible collaborative science through open source, community-curated data packages built on a (pan)genomic foundation. Housed within an integrative software environment, Digital Microbes ensure real-time alignment of research efforts for collaborative teams and facilitate novel scientific insights as new layers of data are added. Here we describe two Digital Microbes: 1) the heterotrophic marine bacterium Ruegeria pomeroyi DSS-3 with >100 transcriptomic datasets from lab and field studies, and 2) the pangenome of the cosmopolitan marine heterotroph Alteromonas containing 339 genomes. Examples demonstrate how an integrated framework collating public (pan)genome-informed data can generate novel and reproducible findings.

bioinformatics↗

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

Metabolite diversity among Prochlorococcus strains belonging to divergent ecotypes

Primary AbstractThe euphotic zone of the surface ocean contains distinct physical-chemical regimes that vary inversely in light and nutrient concentrations as a function of depth. The most numerous phytoplankter of the mid- and low-latitude ocean is the picocyanobacterium Prochlorococcus, which consists of ecologically distinct subpopulations (i.e., "ecotypes"). Ecotypes have different temperature, light and nutrient optima and display distinct relative abundances along gradients of these niche dimensions. As a primary producer, Prochlorococcus fixes and releases organic carbon to neighboring microbes as part of the microbial loop. However, little is known about the specific molecules Prochlorococcus accumulates and releases or how these processes vary among its ecotypes. Here we characterize metabolite diversity of Prochlorococcus by profiling three ecologically-distinct cultured strains: MIT9301, representing a high-light adapted ecotype dominating shallow tropical and sub-tropical waters, MIT0801, representing a low-light adapted ecotype found throughout the euphotic zone and MIT9313, representing a low-light adapted ecotype relatively most abundant at the base of the euphotic zone. In both intracellular and extracellular metabolite profiles, we observe striking differences across strains in the accumulation and release of molecules. Some differences reflect variable genome content across the strains, while others likely reflect variable regulation of genetically-conserved pathways. In the extracellular profiles, we identify molecules that may serve as currencies in Prochlorococcus interactions with neighboring microbes and therefore merit further investigation. ImportanceApproximately half of the annual carbon fixation on Earth occurs in the surface ocean through the photosynthetic activities of phytoplankton such as the ubiquitous picocyanobacterium Prochlorococcus. Ecologically-distinct subpopulations of Prochlorococcus (or ecotypes) are central conduits of organic substrates into the ocean microbiome, thus playing important roles in surface ocean production. By measuring the chemical profile of three cultured ecotype strains, we observed striking differences in the likely chemical impact of Prochlorococcus subpopulations on their surroundings. Subpopulations differ along gradients of temperature, light and nutrient concentrations, suggesting that these chemical differences could affect carbon cycling in different ocean strata and should be considered in models of Prochlorococcus physiology and marine carbon dynamics.

microbiology↗

bioRxiv2022

Chitin utilization by marine picocyanobacteria and the evolution of a planktonic lifestyle

Marine picocyanobacteria (Prochlorococcus and Synechococcus), the most abundant photosynthetic cells in the oceans, are generally thought to have a primarily single-celled and free-living lifestyle. However, we find that genes for breaking down chitin - an abundant source of organic carbon that primarily exists as particles - are widespread in this group. We further show that cells with a chitin degradation pathway display chitin degradation activity, attach to chitin particles and show enhanced growth under low light conditions when exposed to chitosan, a partially deacetylated form of chitin. Marine chitin is largely derived from arthropods, whose roots lie in the early Phanerozoic, 520-535 million years ago, close to when marine picocyanobacteria began colonizing the ocean. We postulate that attachment to chitin particles allowed benthic cyanobacteria to emulate their mat-based lifestyle in the water column, initiating their expansion into the open ocean, seeding the rise of modern marine ecosystems. Transitioning to a constitutive planktonic life without chitin associations along a major early branch within the Prochlorococcus tree led to cellular and genomic streamlining. Our work highlights how coevolution across trophic levels creates metabolic opportunities and drives biospheric expansions.

ecology↗

bioRxiv2018

Emergence of trait variability through the lens of nitrogen assimilation in Prochlorococcus

Intraspecific trait variability has important consequences for the function and stability of marine ecosystems. The marine cyanobacterium Prochlorococcus is a useful model system for understanding how trait variability emerges within microbial species: Its functional diversity is overlaid on measurable environmental gradients, providing a powerful lens into large-scale evolutionary processes. Here we examine variation in the ability to use nitrate across hundreds of Prochlorococcus genomes to better understand the modes of evolution influencing the allocation of ecologically important functions within microbial species. We find that nitrate assimilation genes are absent in basal lineages of Prochlorococcus but occur at an intermediate frequency that is randomly distributed within recently emerged clades. The distribution of nitrate assimilation genes within clades appears largely governed by vertical inheritance, stochastic gene loss, and homologous recombination among closely related cells. By mapping this process onto a model of Prochlorococcus macroevolution, we propose that niche-constructing adaptive radiations and subsequent niche partitioning set the stage for loss of nitrate assimilation genes from basal lineages as they specialized to lower light levels. Retention of these genes in recently emerged lineages has likely been facilitated by selection as they sequentially partitioned into niches where nitrate assimilation conferred a fitness benefit.

evolutionary biology↗