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McCain, J. S. P.

Publications and source records attributed to McCain, J. S. P..

5 recordsLinked to original sources

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↗

Superoxide dismutases shape manganese stoichiometry in Southern Ocean diatoms

Elemental stoichiometry of biomass is a focal point that connects different biogeochemical cycles. Yet, the mechanistic underpinnings of elemental stoichiometry are poorly quantified in many cases. We combined targeted and untargeted metaproteomics, Bayesian statistical modelling, and geochemical measurements to quantify the contribution of specific proteins to metal stoichiometry in natural populations of Southern Ocean diatoms. Our analyses indicate that a substantial amount of non-photosynthetic manganese (Mn) in diatoms in an Antarctic polynya can be attributed to superoxide dismutases ([~]0.7 {micro}mol Mn: mol Carbon; [~]20% of the total cellular Mn quota). We then used cultures and proteomic profiling of the key polar diatom Fragilariopsis cylindrus to identify environmental controls on superoxide dismutases, and discovered that iron concentration has little influence on the abundance of two Mn superoxide dismutases, while Mn limitation induces the depletion of these Mn superoxide dismutases and an accompanying increase of nickel superoxide dismutase. Overall, we combined metaproteomic approaches to quantify proteomic composition and connected these measurements to metal-to-carbon ratios and their responses to metal availability. Because metal quotas are key parameters in some biogeochemical models, our approach provides a direct mechanism for informing ecosystem-scale models with molecular measurements.

microbiology↗

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↗

Proteomic traits vary across taxa in a coastal Antarctic phytoplankton bloom

Production and use of proteins is under strong selection in microbes, but its unclear how proteome-level traits relate to ecological strategies. We identified and quantified proteomic traits of eukaryotic and prokaryotic microbes through an Antarctic phytoplankton bloom using in situ metaproteomics. To do this, we first used simulations, cultures, and bioinformatic methods to rigorously assess our inferences about various proteomic traits and use these assessments to provide several practical recommendations for researchers using metaproteomics. Different taxa, rather than different environmental conditions, formed distinct clusters based on their ribosomal and photosynthetic proteomic proportions, and we propose that these characteristics relate to ecological differences. We defined and used a proteomic proxy for regulatory cost, which showed that SAR11 had the lowest regulatory cost of any taxa we observed at our summertime Southern Ocean study site. Haptophytes had lower regulatory cost than diatoms, which may underpin haptophyte-to-diatom bloom progression in the Ross Sea. Using metaproteomics, we have quantified several proteomic traits (ribosomal and photosynthetic proteomic proportions, regulatory cost) in eukaryotic and prokaryotic taxa, which can then be incorporated into trait-based models of microbial communities that reflect resource allocation strategies.

microbiology↗

Molecular underpinnings and biogeochemical consequences of enhanced diatom growth in a warming Southern Ocean

The Southern Ocean (SO) harbours some of the most intense phytoplankton blooms on Earth. Changes in temperature and iron availability are expected to alter the intensity of SO phytoplankton blooms, but little is known about how environmental change will influence community composition and downstream biogeochemical processes. We performed experimental manipulations on surface ocean microbial communities from McMurdo Sound in the Ross Sea, with and without iron addition, at −0.5 °C, 3 °C, and 6 °C. We then examined nutrient uptake patterns as well as the growth and molecular responses of two dominant diatoms, Fragilariopsis and Pseudo-nitzschia, to these conditions. We found that nitrate uptake and primary productivity were elevated at increased temperature in the absence of iron addition, and were even greater at high temperature with added iron. Pseudo-nitzschia became more abundant under increased temperature without added iron, while Fragilariopsis required additional iron to benefit from warming. We attribute the apparent advantage Pseudo-nitzschia shows under warming to upregulation of iron-conserving photosynthetic processes, utilization of iron-economic nitrogen assimilation mechanisms, and increased iron uptake and storage. These data identify important molecular and physiological differences between dominant diatom groups and add to the growing body of evidence for Pseudo-nitzschia’s increasingly important role in warming SO ecosystems. This study also suggests that temperature-driven shifts in SO phytoplankton assemblages may increase utilization of the vast pool of excess nutrients in iron-limited SO surface waters, and thereby influence global nutrient distributions and carbon cycle.Significance Statement Phytoplankton assemblages contribute to the Southern Ocean’s ability to absorb atmospheric CO2, form the base of marine food webs, and shape the global distribution of macronutrients. Anthropogenic climate change is altering the SO environment, yet we do not fully understand how resident phytoplankton will react to this change. By comparing the responses of two prominent SO diatom groups to changes in temperature and iron in a natural community, we find that one group, Pseudo-nitzschia, grows better under warmer low-iron conditions by managing cellular iron demand and efficiently increasing photosynthetic capacity. This ability to grow and draw down nutrients in the face of warming, regardless of iron availability, may have major implications for ocean ecosystems and global nutrient and carbon cycles.Competing Interest StatementThe authors have declared no competing interest.View Full Text

ecology↗