Biology subjects

Levine, N. M.

Publications and source records attributed to Levine, N. M..

14 recordsLinked to original sources

bioRxiv2026

Macro evolutionary patterns do not predict micro evolutionary trajectories

As the worlds oceans change in response to climate change, phytoplankton communities will adapt to warmer, more stratified surface waters via plasticity, evolution, and range shifts. Current global ocean models assume that size structured phytoplankton communities have fixed trait relationships, and as a result generally predict that smaller size classes will become more dominant globally. However, this general expectation fails to consider how intra-species trait tradeoffs may operate orthogonally from large-scale inter-species tradeoffs--allowing for alternative evolutionary pathways given the limits and/or possibilities available to ancestral populations. To identify evolutionary pathways phytoplankton populations might take, we develop a novel modeling framework that combines a trait-based phytoplankton quota model with stochastic evolution (ecoTRACE). EcoTRACE explicitly decouples key phytoplankton traits from interspecific allometric relationships, allowing for novel phenotypes to emerge. We validated ecoTRACE against a long-term artificial size selection experiment on Dunaliella tertiolecta. We show that ecoTRACE captures multi-dimensional evolved phenotypes that quota models based on interspecific relationships fail to reproduce. Under fluctuating multi-stressor growth, model populations evolve phenotypic plasticity that deviates from predicted interspecific allometric relationships. EcoTRACE provides a framework for generating hypotheses as to the evolutionary trajectories that phytoplankton will experience in a warmer, more variable ocean.

microbiology↗

bioRxiv2025

New niches for larger phytoplankton in a warmer, more resource-limited ocean

Warming and nutrient limitation are major stressors that affect primary production in the ocean, with cascading impacts on the food web. Yet, we lack a mechanistic understanding of how phytoplankton manage multiple stressors and the implications of these responses for phytoplankton biogeography. By combining theory, proteome allocation modeling, and climate projections, we identified two potential competing strategies for multi-stressor growth: (1) nutrient efficient smaller cells, or (2) heat-tolerant larger cells. We found that Prochlorococcus are more vulnerable in warmer, "heat-stressed", tropical regions due to greater heat sensitivity and lower lipid storage capacity to buffer oxidative stress, indicating a potential ecological niche for larger phytoplankton with lower sensitivity to oxidative stress, such as Synechococcus and picoeukaryotes. Our findings advocate for the inclusion of phytoplankton heat-stress responses in global models to more accurately predict their ecological niches as the climate warms.

ecology↗

bioRxiv2024

Emergent Metabolic Niches for Marine Heterotrophs

Ocean microbial communities are made up of thousands of diverse taxa whose metabolic demands set the rates of both biomass production and degradation. Thus, these microscopic organisms play a critical role in ecosystem dynamics, global carbon cycling, and climate. While we have frameworks for relating phytoplankton diversity to rates of carbon fixation, our knowledge of how variations in heterotrophic microbial populations drive changes in carbon cycling is in its infancy. Here, we leverage global metagenomic datasets and metabolic models to identify a set of metabolic niches with distinct growth strategies. These groupings provide a simplifying framework for describing microbial communities in different oceanographic regions and for understanding how heterotrophic microbial populations function. This framework, predicated directly on metabolic capability rather than taxonomy, enables us to tractably link heterotrophic diversity directly to biogeochemical rates in large scale ecosystem models.

ecology↗

bioRxiv2024

Predictable functional biogeography of marine microbial heterotrophs

Heterotrophic bacteria and archaea ( heteroprokaryotes) drive global carbon cycling, but how to quantitatively organize their functional complexity remains unclear. We generated a global-scale understanding of marine heteroprokaryotic functional biogeography by synthesizing genetic sequencing data with a mechanistic marine ecosystem model. We incorporated heteroprokaryotic diversity into the trait-based model along two axes: substrate lability and growth strategy. Using genetic sequences along three ocean transects, we compiled 21 heteroprokaryotic guilds and estimated their degree of optimization for rapid growth (copiotrophy). Data and model consistency indicated that gradients in grazing and substrate lability predominantly set biogeographical patterns, and identified deep-ocean slow copiotrophs whose ecological interactions control the surface accumulation of dissolved organic carbon.

ecology↗

bioRxiv2023

Widespread B-vitamin auxotrophy in marine particle-associated bacteria

Microbial community assembly is governed by trophic interactions that mediate the transfer of carbon sources and biomass building blocks between species. However, central metabolism corresponds to only a small fraction of the biosynthetic potential of microbes: metabolites such as antimicrobial compounds, signaling molecules, and co-factors are underexplored forces shaping microbial communities. Here, we focus on B vitamin exchange in coastal marine bacterial communities that degrade particulate organic matter and find that natural seawater communities are vitamin limited. While almost a third of bacterial isolates from these communities are B vitamin auxotrophs, the pioneering degraders that first arrive on particles are vitamin producers that likely support auxotrophs through cross-feeding. However, combining experiments and a resource-explicit model, we show that auxotroph growth is often not restored by coculture with vitamin producers, but rather requires lysis and subsequent vitamin recycling. Our results highlight the importance of vitamin auxotrophies and lysis-mediated cross-feeding as important factors controlling microbial community assembly and succession on marine particles.

microbiology↗

bioRxiv2023

Mechanistic constraints on the trade-off between photosynthesis and respiration in response to warming

Phytoplankton are responsible for half of all oxygen production and drive the ocean carbon cycle. Metabolic theory predicts that increasing global temperatures will cause phytoplankton to become more heterotrophic and smaller. Here we uncover the metabolic trade-offs between cellular space, energy, and stress management driving phytoplankton thermal acclimation and how these might be overcome through evolutionary adaptation. We show that the observed relationships between traits such as chlorophyll, lipid content, C:N and size can be predicted based on the metabolic demands of the cell, the thermal dependency of transporters, and changes in membrane lipids. We suggest that many of the observed relationships are not fixed physiological constraints but rather can be altered through adaptation. For example, the evolution of lipid metabolism can favor larger cells with higher lipid content to mitigate oxidative stress. These results have implications for rates of carbon sequestration and export in a warmer ocean. TeaserA tale of how photosynthetic microbes might defy current trends to become larger and grow faster in a warmer ocean.

cell biology↗

bioRxiv2022

Rapid reductions in population size drive evolutionary divergence in diatoms

Unicellular photosynthetic marine microbes, or phytoplankton, make up the base of marine food webs and drive global nutrient cycles. Despite their key roles in ecology and biogeochemistry, we have a limited understanding of how the basic features of their demographics along with dynamic environments affect trait evolution. A key feature of diatom ecology is frequent extreme reductions in population size, both as part of their bloom-and-bust growth dynamics, and as a result of living within ocean currents. Here, we use experimental evolution to understand which metabolic pathways and functions readily diversify in diatom populations following population bottleneck events. We subjected replicate populations of six genetically distinct diatom strains to population bottlenecks and then subsequently allowed them to evolve as large populations in the absence of environmental change. Phylogenies and global expression of orthologs were generally strain-specific, indicating that vertical (inherited) evolutionary constraints largely determine the occupation of specific locations in the transcriptional landscape (i.e. tran-scape). Following bottlenecks and subsequent evolution as large populations, transcriptional networks of most populations returned to those of the ancestral population. However, at least one replicate population per lineage migrated in the tran-scape, demonstrating that evolutionary changes in gene expression patterns and transcriptional relationships can be driven by population bottlenecks even in the absence of environmental change. Importantly, the orthologs dominating transcriptional diversification resided in common, central metabolic pathways. These data advance our understanding of constraints and patterns of transcriptional relationships underlying trait evolution in microbes that drive global food webs and elemental cycles.

evolutionary biology↗

bioRxiv2022

How connected are different multitrait phenotypes in a model diatom genus?

Phytoplankton are photosynthetic marine microbes that affect food webs, nutrient cycles, and climate regulation. Their roles are determined by a correlated set of phytoplankton functional traits including cell size, chlorophyll content, and cellular composition. Here, we explore how interrelated trait values and correlations evolve. Because both chance events and natural selection contribute to phytoplankton trait evolution, we used population bottlenecks to diversify six genotypes of Thalassiosirid diatoms. We then evolved them in two environments where natural selection could act on this diversity. Interspecific variation and within-species evolution were visualized for nine traits and their correlations using reduced axes (a trait-scape). Shifts in both trait values and correlations, resulting in movement of evolving populations on the trait-scape, occurred in both environments, and were more frequent under environmental change. Which trait correlations evolved was strain-specific, but greater departures from ancestral trait correlations were associated with lower population growth rates. There was no single master trait that could be used to understand multitrait evolution. Instead, repeatable multitrait evolution occurred along a major axis of variation defined by several diatom functional traits and trait relationships. Because trait-scapes capture changes in trait correlations and values together, they offer an insightful way to study multitrait variation.

evolutionary biology↗

bioRxiv2021

Bacterial chemotaxis to saccharides is governed by a trade-off between sensing and uptake

To swim up gradients of nutrients, E. coli senses nutrient concentrations within its periplasm. For small nutrient molecules, periplasmic concentrations typically match extracellular concentrations. However, this is not necessarily the case for saccharides, such as maltose, which is transported into the periplasm via a specific porin. Previous observations have shown that under various conditions E. coli limits maltoporin abundance so that, for extracellular micromolar concentrations of maltose, there are predicted to be only nanomolar concentrations of free maltose in the periplasm. Thus, in the micromolar regime, the total uptake of maltose from the external environment into the cytoplasm is limited not by the abundance of cytoplasmic transport proteins but by the abundance of maltoporins. Here we present results from experiments and modeling showing that this porin-limited transport enables E. coli to sense micromolar gradients of maltose despite having a high-affinity ABC transport system that is saturated at these micromolar levels. We used microfluidic assays to study chemotaxis of E. coli in various gradients of maltose and methyl-aspartate and leveraged our experimental observations to develop a mechanistic transport-and-sensing chemotaxis model. Incorporating this model into agent-based simulations, we discover a trade-off between uptake and sensing: although high-affinity transport enables higher uptake rates at low nutrient concentrations, it severely limits dynamic sensing range. We thus propose that E. coli may limit periplasmic uptake to increase its chemotactic sensitivity, enabling it to use maltose as an environmental cue. Statement of SignificanceBacterial chemotaxis is among the best-studied systems in biology and is paradigmatic of the mechanisms used by cells to link sensory inputs with regulated responses, thus providing insight into the ecological basis of cellular physiology. Here we present a mechanistic chemotaxis model that describes how the regulation of the transport of a sugar into and out of the cells periplasm affects the cells motile response to that sugar. Based on observations from population-level chemotaxis assays, we uncover an ecologically relevant trade-off between sensing and uptake. The general finding of this work is that, while high-affinity transport allows for higher uptake rates, it can severely limit the cells dynamic sensing range.

microbiology↗

bioRxiv2020

Mechanistic model of nutrient uptake explains dichotomy between marine oligotrophic and copiotrophic bacteria

Marine heterotrophic bacteria use a spectrum of nutrient uptake strategies, from that of copiotrophs--which dominate in nutrient-rich environments--to that of oligotrophs--which dominate in nutrient-poor environments. While copiotrophs possess numerous phosphotransferase systems (PTS), oligotrophs lack PTS and rely on ATP-binding cassette (ABC) transporters, which use binding proteins. Here we present a molecular-level model that explains the dichotomy between oligotrophs and copiotrophs as the consequence of trade-offs between PTS and ABC transport. When we approximate ABC transport in Michaelis-Menten form, we find, contrary to the canonical formulation, that its half-saturation concentration KM is not a constant but instead a function of binding protein abundance. Thus, oligotrophs can attain nanomolar KM values using binding proteins with micromolar dissociation constants and while closely matching transport and metabolic capacities. However, this requires large periplasms and high abundances of binding proteins, whose slow diffusion limits uptake rate. We conclude that the use of binding proteins is critical for oligotrophic survival yet severely constrains maximal growth rates, thus fundamentally shaping the divergent evolution of oligotrophs and copiotrophs.

microbiology↗

bioRxiv2020

A unified theory for organic matter accumulation

Organic matter constitutes a key reservoir in global elemental cycles. However, our understanding of the dynamics of organic matter and its accumulation remains incomplete. Seemingly disparate hypotheses have been proposed to explain organic matter accumulation: the slow degradation of intrinsically recalcitrant substrates, the depletion to concentrations that inhibit microbial consumption, and a dependency on the consumption capabilities of nearby microbial populations. Here, using a mechanistic model, we develop a theoretical framework that explains how organic matter predictably accumulates in natural environments due to biochemical, ecological, and environmental factors. The new framework subsumes the previous hypotheses. Changes in the microbial community or the environment can move a class of organic matter from a state of functional recalcitrance to a state of depletion by microbial consumers. The model explains the vertical profile of dissolved organic carbon in the ocean and connects microbial activity at subannual timescales to organic matter turnover at millenial timescales. The threshold behavior of the model implies that organic matter accumulation may respond nonlinearly to changes in temperature and other factors, providing hypotheses for the observed correlations between organic carbon reservoirs and temperature in past earth climates.

ecology↗

bioRxiv2020

Evolving trait correlations underlie multi-trait adaptation in a eukaryotic alga

Microbes form the base of food webs and drive biogeochemical cycling. Predicting the effects of microbial evolution on global elemental cycles remains a significant challenge due to the sheer number of interacting environmental and trait combinations. Here we present an approach for integrating multivariate trait data into a predictive model of trait evolution. We investigated the outcome of thousands of possible adaptive walks parameterized using empirical evolution data from the alga Chlamydomonas exposed to high CO2. We found that the direction of historical bias (existing trait correlations) influenced both the rate of adaptation and the evolved phenotypes (trait combinations). Critically, we use fitness landscapes derived directly from empirical trait values to capture known evolutionary phenomena. This work demonstrates that ecological models need to represent both changes in traits and changes in the correlation between traits in order to accurately capture phytoplankton evolution and predict future shifts in elemental cycling.

microbiology↗

bioRxiv2019

Hitting a moving target: Microbial evolutionary strategies in a dynamic ocean

Marine microbes form the base of ocean food webs and drive ocean biogeochemical cycling. Yet little is known about how microbial populations will evolve due to global change-driven shifts in ocean dynamics. Understanding adaptive timescales is critical where long-term trends (e.g. warming) are coupled to shorter-term advection dynamics that move organisms rapidly between ecoregions. Here we investigated the interplay between physical and biological timescales using a model of adaptation and an eddy-resolving ocean circulation climate model. Two criteria ( and {beta}) were identified that relate physical and biological timescales and determine the timing and nature of adaptation. Genetic adaptation was impeded in highly variable regimes (<1) but promoted in more stable environments (>1). An evolutionary trade-off emerged where greater short-term transgenerational effects (low-{beta}-strategy) enabled rapid responses to environmental fluctuations but delayed genetic adaptation, while fewer short-term transgenerational effects (high-{beta}-strategy) allowed faster genetic adaptation but inhibited short-term responses. Our results suggest that organisms with faster growth rates are better positioned to adapt to rapidly changing ocean conditions and that more variable environments will favor a bet-hedging, low-{beta}-strategy. Understanding the relationship between evolutionary and physical timescales is critical for robust predictions of future microbial dynamics.

evolutionary biology↗

bioRxiv2017

Marine proteorhodopsins rival photosynthesis in solar energy capture

All known phototrophic metabolisms on Earth are based on one of three energy-converting pigments: chlorophyll-a, bacteriochlorophyll-a, and retinal, which is the chromophore in rhodopsins [1]. While the contribution of chlorophylls to global energy flows and marine carbon cycling has been studied for decades, the role of retinal-based phototrophy remains largely unexplored [1,2]. We report the first vertical distributions of the three energy-converting pigments measured along a contrasting nutrient gradient through the Mediterranean Sea and the Eastern Atlantic Ocean. The highest proteorhodopsin concentrations were observed above the deep chlorophyll-a maxima, and their geographical distribution tended to be inversely related to that of chlorophyll-a. We further show that proteorhodopsins potentially absorb as much or more light energy than chlorophyll-a -based phototrophy and this energy is sufficient to sustain bacterial basal metabolism. Our results suggest that ubiquitous proteorhodopsin-containing heterotrophs are important contributors to the light energy captured in the sea.

ecology↗