Biology subjects

Follows, M. J.

Publications and source records attributed to Follows, M. J..

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↗

bioRxiv2026

Nutrient response strategies drive coastal range shifts of phytoplankton taxa

Coastal phytoplankton blooms are important drivers of regional and global marine primary production. Recently documented increases in coastal phytoplankton blooms in the first quarter of the 21st century may be a consequence in part of changing environmental conditions and have important ecological implications. Here, we explore coastal phytoplankton dynamics in Cape Cod Bay, MA, USA. We use a 20-year phytoplankton ecology dataset to identify potential drivers of the increasing prevalence of two regionally-rare phytoplankton taxa: a coccolithophore thought to thrive in the global open ocean, and a dinoflagellate genus with potentially toxic members. Using metatranscriptomics, we show that these minor phytoplankton taxa leverage unique strategies to gain a competitive advantage under nutrient limitation compared to traditionally dominant taxa and compared to a diatom taxon that became modestly more abundant over the study period. Our results highlight the ecological dynamics arising from long-term shifts in temperature and nutrient status in coastal ecosystems.

ecology↗

bioRxiv2025

Cellular-level control on global ocean deoxygenation driven by phytoplankton ecophysiology

Phytoplankton elemental composition shapes the distribution of dissolved nutrient concentrations and thus plays a key role in ocean biogeochemistry. While the carbon-to-nitrogen-to-phosphorus ratio (C:N:P) in marine phytoplankton has been extensively studied, the hydrogen (H) and oxygen (O) content have received less attention despite their critical role in determining dissolved oxygen (O2) consumption rates in the ocean. Here, we estimated the elemental composition of marine phytoplankton, including the H and O content, from first principles, using a cellular allocation model embedded in a global ocean model. We estimated that an average phytoplankton cell has a chemical formula of C107H190N16O53P, with an O2 demand of 149 mol O2/mol P and respiration quotients of 1.40 mol O2/mol C, suggesting a lower H and O content, and higher O2 demand than commonly assumed. We found global variations in the O2 demand of organic matter respiration driven by population structure and cellular reorganisation under different environmental conditions. By testing how shifts in the macromolecular composition of phytoplankton cells affect the oceans O2 budget, we found that O2 consumption increases significantly when shifting cell composition from carbohydrate-rich to protein- or lipid-rich cells. As a result, low-O2 (hypoxic) zones in the ocean expanded by 75%. These findings demonstrate that cellular-level processes in marine phytoplankton shape the global O2 cycle and large-scale patterns of ocean biogeochemistry.

ecology↗

bioRxiv2024

Microbial reaction rate estimation using proteins and proteomes

Microbes transform their environments using diverse enzymatic reactions. However, it remains challenging to measure microbial reaction rates in natural environments. Despite advances in global quantification of enzyme abundances, the individual relationships between enzyme abundances and their reaction rates have not been systematically examined. Using matched proteomic and reaction rate data from microbial cultures, we show that enzyme abundance is often insufficient to predict its corresponding reaction rate. However, we discovered that global proteomic measurements can be used to make accurate rate predictions of individual reaction rates (median R2 = 0.78). Accurate rate predictions required only a small number of proteins and they did not need explicit prior mechanistic knowledge or environmental context. These results indicate that proteomes are encoders of cellular reaction rates, potentially enabling proteomic measurements in situ to estimate the rates of microbially mediated reactions in natural systems. SignificanceOne of the most basic phenotypes of a microbe is its set of associated reaction rates, but quantifying these rates in situ remains extremely challenging, especially in natural systems. We used molecular data and statistical models to estimate microbial rates in steady state cultures. We found that many reaction rates are highly predictable using proteomic data, though single proteins are typically not informative for their associated reaction rates. This result suggests that gene expression data from complex microbial communities could be used to estimate in situ reaction rates, providing new clues into the lives and environmental function of microbes.

systems biology↗

bioRxiv2024

Intraspecific diversity in thermal performance determines phytoplankton ecological niche

Temperature has a primary influence on phytoplankton physiology and affects biodiversity and ecology. To examine how intraspecific diversity and temperature shape plankton populations, we grew 12 strains of the ecologically-important coccolithophore Gephyrocapsa huxleyi isolated from regions of different temperature for [~]45 generations (2 months), each at 6-8 temperatures, and characterized the acclimated thermal response curve of each strain. Even with virtually identical temperature optima and overlapping cell size, strain growth rates varied between 0.45 and 1 day-1. While some thermal curves were effectively symmetrical, others had more slowly declining growth rates above the "thermal optimum," and thermal niche widths varied between 16.7 and 24.8 {degrees}C. This suggests that different strains use distinct thermal response mechanisms. We investigated the ecological implications of such intraspecific diversity on thermal response using an ocean ecosystem simulation resolving distinct phytoplankton thermal phenotypes. Resolving model analogs of thermal "generalists" and "specialists" (similar to those observed in G. huxleyi) resulted in a distinctive global biogeography of preferred thermal niche widths with a nonlinear latitudinal pattern. We leveraged the model output to predict the ranges of the 12 strains we studied in the laboratory and demonstrated how this approach could refine predictions of phytoplankton thermal geographic range in situ. Our combination of observed thermal traits and modeled biogeography highlights the capacity of diverse groups to persist through temperature shifts. Significance StatementIntraspecific diversity in the phytoplankton may underpin their distribution. We show that within a single coccolithophore species, thermal response curves have diverse trait parameters. For example, many strains had a variable range of temperatures at which they could survive (thermal niche width). Adding this thermal niche width diversity to an ecosystem model simulation impacted phytoplankton coexistence and overall biomass. These observations show that thermal niche width is a gap in phytoplankton representation in ecosystem models that impacts modeled phytoplankton biogeography and concomitant carbon cycle dynamics. Including thermal tolerance is crucial to predictive modeling as ocean temperature dynamics change.

ecology↗

bioRxiv2023

Missing microbial eukaryotes and misleading meta-omic conclusions

Meta-omics has become commonplace in the study of microbial eukaryotes. The explosion of available data has inspired large-scale analyses, including species or taxonomic group distribution mapping, gene catalog construction, and inference on the functional roles and activities of microbial eukaryotes in situ. However, genome and transcriptome databases are prone to misannotation biases, and meta-omic inventories may have no recoverable taxonomic annotation for more than half of assembled contigs or predicted proteins. Direct mapping solely to organisms of interest might introduce a problematic misattribution bias, while full databases can annotate any cataloged organism but may be imbalanced between taxa. Here, we explore the potential pitfalls of common approaches to taxonomic annotation of protistan meta-omic datasets. We argue that ongoing curation of genetic resources is critical in accurately annotating protists in situ in meta-omic datasets. Moreover, we propose that precise taxonomic annotation of meta-omic data is a clustering problem rather than a feasible alignment problem. We show that taxonomic membership of sequence clusters demonstrates more accurate estimated community composition than returning exact sequence labels, and overlap between clusters can address database shortcomings. Clustering approaches can be applied to diverse environments while continuing to exploit the wealth of annotation data collated in databases, and database selection and evaluation is a critical part of correctly annotating protistan taxonomy in environmental datasets. We re-analyze three environmental datasets at three levels of taxonomic hierarchy in order to illustrate the critical importance of both database completeness and curation in enabling accurate environmental interpretation.

microbiology↗

bioRxiv2022

Reverse engineering environmental metatranscriptomes clarifies best practices for eukaryotic assembly

Diverse communities of microbial eukaryotes in the global ocean provide a variety of essential ecosystem services, from primary production and carbon flow through trophic transfer to cooperation via symbioses. Increasingly, these communities are being understood through the lens of omics tools, which enable high-throughput processing of communities of multiple species. Metatranscriptomics in particular offers an understanding of real-time gene expression in microbial eukaryotic communities, providing a window into community metabolic activity. However, these approaches are rarely validated. A systematic validation of metatranscriptome assembly and annotation methods is necessary to appropriately assess (1) the fidelity of our community composition measurements and (2) the confidence of novel taxonomic and functional content discovered with metatranscriptomics. Here, we present euk rhythmic, an automated and customizable multi-assembler workflow for eukaryotic metatranscriptome assembly, annotation, and analysis, and validate the ability of the pipeline to recapitulate simulated eukaryotic community-level expression data treated as a gold standard. Finally, we apply this pipeline to two previously published metatranscriptomic datasets, showing both recapitulation of previous results as well as enhanced taxonomic and functional gene discovery.

bioinformatics↗

bioRxiv2022

Significant organic carbon acquisition by Prochlorococcus in the oceans

Marine phytoplankton are responsible for about half of the photosynthesis on Earth. Many are mixotrophs, combining photosynthesis with heterotrophic assimilation of organic carbon but the relative contribution of these two carbon sources is not well quantified. Here, single-cell measurements reveal that Prochlorococcus at the base of the photic zone in the Eastern Mediterranean Sea are obtaining only ~20% of carbon required for growth by photosynthesis. Consistently, laboratory-calibrated evaluations of Prochlorococcus photosynthesis indicate that carbon fixation is systematically too low to support published in situ growth rates in the deep photic layer of the Pacific Ocean. Furthermore, agent-based model simulations show that mixotrophic cells maintain realistic growth rates and populations 10s of meters deeper than obligate photo-autotrophs, deepening the nutricline and Deep Chlorophyll Maximum by ~20 m. Time-series of Prochlorococcus ecotype-abundance from the subtropical North Atlantic and North Pacific suggest that up to 30% of the Prochlorococcus cells live where light intensity is not enough to sustain obligate photo-autotrophic populations during warm, stratified periods. Together, these data and models suggest that mixotrophy underpins the ecological success of a large fraction of the global Prochlorococcus population and its collective genetic diversity.

microbiology↗

bioRxiv2021

Diel population dynamics and mortality of Prochlorococcus in the North Pacific Subtropical Gyre

Photosynthesis fuels primary production at the base of marine food webs. Yet, in many surface ocean ecosystems, diel-driven primary production is tightly coupled to daily loss. This tight coupling raises the question: which top-down drivers predominate in maintaining persistently stable picocyanobacterial populations over longer time scales? Motivated by high-frequency surface water measurements taken in the North Pacific Subtropical Gyre (NPSG), we developed multitrophic models to investigate bottom-up and top-down mechanisms underlying the balanced control of Prochlorococcus populations. We find that incorporating photosynthetic growth with viral- and predator-induced mortality is sufficient to recapitulate daily oscillations of Prochlorococcus abundances with baseline community abundances. In doing so, we infer that grazers function as the primary top-down factor despite high standing viral particle densities while identifying the potential for light-dependent viral traits and non-canonical loss factors to shape the structure and function of marine microbial communities.

ecology↗

bioRxiv2021

Diel light cycles affect phytoplankton competition in the global ocean

Light, essential for photosynthesis, is present in two periodic cycles in nature: seasonal and diel. Although seasonality of light is typically resolved in ocean ecosystem and biogeochemistry models because of its significance for seasonal succession and biogeography of phytoplankton, the diel light cycle is generally not resolved. Here we use a three-dimensional global ocean model and compare high temporal resolution simulations with and without diel light cycles. The model simulates 15 phytoplankton types of different cell size, encompassing two broad ecological strategies: small cells with high nutrient affinity (gleaners) and larger cells with high maximal growth rate (opportunists). Both are grazed by zooplankton and limited by nitrogen, phosphorus and iron. Simulations show that diel cycles of light induce diel cycles in phytoplankton populations and limiting nutrients in the global ocean. Diel nutrient cycles are associated with higher concentration of limiting nutrients by up to 200% at low latitudes (-40{degrees} to 40{degrees}), a process that increases opportunists biomass by up to 50%. Size classes with the highest maximal growth rates from both gleaner and opportunist groups are favored the most by diel light cycles. This mechanism weakens as latitude increases because the effects of the seasonal cycle dominate over those of the diel cycle. The present work shows that resource competition under diel light cycles has a significant impact on phytoplankton biogeography, indicating the necessity of resolving diel processes in global ocean models.

ecology↗

bioRxiv2019

Dynamic macromolecular composition and high exudation rates in Prochlorococcus

Every living cell is composed of macromolecules such as proteins, DNA, RNA and pigments. The ratio between these macromolecular pools depends on the allocation of resources within the organism to different physiological requirements, and in turn affects biogeochemical cycles of elements such as carbon, nitrogen and phosphorus. Here, we present detailed measurements of the macromolecular composition of Prochlorococcus MIT9312, a representative strain of a globally abundant marine primary producer, as it grows and declines due to nitrogen starvation in laboratory batch cultures. As cells reached stationary stage and declined, protein per cell decreased by [~]30% whereas RNA per cell and pigments per cell decreased by [~]75%. The decline stage was associated with the appearance of chlorotic cells which had higher forward scatter (a proxy for cell size) but lower chlorophyll autofluorescence, as well as with changes in photosynthetic pigment composition. Specifically, during culture decline divinyl-chlorophyll-like pigments emerged, which were not observed during exponential growth. These divinyl-chlorophyll-like pigments were also observed in natural samples from the Eastern Mediterranean. Around >80% of the carbon fixed by Prochlorococcus MIT9312 (but not of a different strain, NATL2A) was released into the growth media as dissolved organic carbon under these laboratory conditions. Variations in RNA/protein indicate that, broadly defined, the macromolecular composition of Prochlorococcus MIT9312 is more similar to eukaryotic phytoplankton than to marine heterotrophic bacteria, possibly due to the significant investment in photosynthetic machinery of phototrophs.

microbiology↗