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ABSTRACT Microorganisms grow despite imbalances in the availability of nutrients and energy. The biochemical and elemental adjustments that bacteria employ to sustain growth when these resources are suboptimal are not well understood. We assessed howPseudomonas putidaKT2440 adjusts its physiology at differing dilution rates (to approximate growth rates) in response to carbon (C), nitrogen (N), and phosphorus (P) stress using chemostats. Cellular elemental and biomolecular pools were variable in response to different limiting resources at a slow dilution rate of 0.12 h⁻¹, but these pools were more similar across treatments at a faster rate of 0.48 h⁻¹. At slow dilution rates, limitation by P and C appeared to alter cell growth efficiencies as reflected by changes in cellular C quotas and rates of oxygen consumption, both of which were highest under P- and lowest under C- stress. Underlying these phenotypic changes was differential gene expression of terminal oxidases used for ATP generation that allows for increased energy generation efficiency. In all treatments under fast dilution rates, KT2440 formed aggregates and biofilms, a physiological response that hindered an accurate assessment of growth rate, but which could serve as a mechanism that allows cells to remain in conditions where growth is favorable. Our findings highlight the ways that microorganisms dynamically adjust their physiology under different resource supply conditions, with distinct mechanisms depending on the limiting resource at slow growth and convergence toward an aggregative phenotype with similar compositions under conditions that attempt to force fast growth. IMPORTANCEAll organisms experience suboptimal growth conditions due to low nutrient and energy availability. Their ability to survive and reproduce under such conditions determines their evolutionary fitness. By imposing suboptimal resource ratios under different dilution rates on the model organismPseudomonas putidaKT2440, we show that this bacterium dynamically adjusts its elemental composition, morphology, pools of biomolecules, and levels of gene expression. By examining the ability of bacteria to respond to C:N:P imbalance, we can begin to understand how stoichiometric flexibility manifests at the cellular level and impacts the flow of energy and elements through ecosystems. 

Abstract BackgroundThroughout its nearly four-billion-year history, life has undergone evolutionary transitions in which simpler subunits have become integrated to form a more complex whole. Many of these transitions opened the door to innovations that resulted in increased biodiversity and/or organismal efficiency. The evolution of multicellularity from unicellular forms represents one such transition, one that paved the way for cellular differentiation, including differentiation of male and female gametes. A useful model for studying the evolution of multicellularity and cellular differentiation is the volvocine algae, a clade of freshwater green algae whose members range from unicellular to colonial, from undifferentiated to completely differentiated, and whose gamete types can be isogamous, anisogamous, or oogamous. To better understand how multicellularity, differentiation, and gametes evolved in this group, we used comparative genomics and fossil data to establish a geologically calibrated roadmap of when these innovations occurred. ResultsOur ancestral-state reconstructions, show that multicellularity arose independently twice in the volvocine algae. Our chronograms indicate multicellularity evolved during the Carboniferous-Triassic periods in Goniaceae + Volvocaceae, and possibly as early as the Cretaceous in Tetrabaenaceae. Using divergence time estimates we inferred when, and in what order, specific developmental changes occurred that led to differentiated multicellularity and oogamy. We find that in the volvocine algae the temporal sequence of developmental changes leading to differentiated multicellularity is much as proposed by David Kirk, and that multicellularity is correlated with the acquisition of anisogamy and oogamy. Lastly, morphological, molecular, and divergence time data suggest the possibility of cryptic species in Tetrabaenaceae. ConclusionsLarge molecular datasets and robust phylogenetic methods are bringing the evolutionary history of the volvocine algae more sharply into focus. Mounting evidence suggests that extant species in this group are the result of two independent origins of multicellularity and multiple independent origins of cell differentiation. Also, the origin of the Tetrabaenaceae-Goniaceae-Volvocaceae clade may be much older than previously thought. Finally, the possibility of cryptic species in the Tetrabaenaceae provides an exciting opportunity to study the recent divergence of lineages adapted to live in very different thermal environments. 

Abstract With the ongoing differential disruption of the biogeochemical cycles of major elements that are essential for all life (carbon, nitrogen, and phosphorus), organisms are increasingly faced with a heterogenous supply of these elements in nature. Given that photosynthetic primary producers form the base of aquatic food webs, impacts of changed elemental supply on these organisms are particularly important. One way that phytoplankton cope with the differential availability of nutrients is through physiological changes, resulting in plasticity in macromolecular and elemental biomass composition. Here, we assessed how the green algaChlamydomonas reinhardtiiadjusts its macromolecular (e.g., carbohydrates, lipids, and proteins) and elemental (C, N, and P) biomass pools in response to changes in growth rate and the modification of resources (nutrients and light). We observed thatChlamydomonasexhibits considerable plasticity in elemental composition (e.g., molar ratios ranging from 124 to 971 for C:P, 4.5 to 25.9 for C:N, and 15.1 to 61.2 for N:P) under all tested conditions, pointing to the adaptive potential ofChlamydomonasin a changing environment. Exposure to low light modified the elemental and macromolecular composition of cells differently than limitation by nutrients. These observed differences, with potential consequences for higher trophic levels, included smaller cells, shifts in C:N and C:P ratios (due to proportionally greater N and P contents), and differential allocation of C among macromolecular pools (proportionally more lipids than carbohydrates) with different energetic value. However, substantial pools of N and P remained unaccounted for, especially at fast growth, indicating accumulation of N and P in forms we did not measure. 

Growth is a function of the net accrual of resources by an organism. Energy and elemental contents of organisms are dynamically linked through their uptake and allocation to biomass production, yet we lack a full understanding of how these dynamics regulate growth rate. Here, we develop a multivariate imbalance framework, the growth efficiency hypothesis, linking organismal resource contents to growth and metabolic use efficiencies, and demonstrate its effectiveness in predicting consumer growth rates under elemental and food quantity limitation. The relative proportions of carbon (%C), nitrogen (%N), phosphorus (%P), and adenosine triphosphate (%ATP) in consumers differed markedly across resource limitation treatments. Differences in their resource composition were linked to systematic changes in stoichiometric use efficiencies, which served to maintain relatively consistent relationships between elemental and ATP content in consumer tissues and optimize biomass production. Overall, these adjustments were quantitatively linked to growth, enabling highly accurate predictions of consumer growth rates.