Metabolic evolution and the self-organization of ecosystems

Abstract

Metabolism mediates the flow of matter and energy through the biosphere. We examined how metabolic evolution shapes ecosystems by reconstructing it in the globally abundant oceanic phytoplankter Prochlorococcus. To understand what drove observed evolutionary patterns, we interpreted them in the context of its population dynamics, growth rate, and light adaptation, and the size and macromolecular and elemental composition of cells. This multilevel view suggests that, over the course of evolution, there was a steady increase in Prochlorococcus' metabolic rate and excretion of organic carbon. We derived a mathematical framework that suggests these adaptations lower the minimal subsistence nutrient concentration of cells, which results in a drawdown of nutrients in oceanic surface waters. This, in turn, increases total ecosystem biomass and promotes the coevolution of all cells in the ecosystem. Additional reconstructions suggest that Prochlorococcus and the dominant cooccurring heterotrophic bacterium SAR11 form a coevolved mutualism that maximizes their collective metabolic rate by recycling organic carbon through complementary excretion and uptake pathways. Moreover, the metabolic codependencies of Prochlorococcus and SAR11 are highly similar to those of chloroplasts and mitochondria within plant cells. These observations lead us to propose a general theory relating metabolic evolution to the self-amplification and selforganization of the biosphere. We discuss the implications of this framework for the evolution of Earth's biogeochemical cycles and the rise of atmospheric oxygen. metabolic evolution | Prochlorococcus | microbial oceanography | mutualism | Earth history M etabolism sustains the nonequilibrium chemical order of the biosphere by continually supplying the energy and building blocks of all cells on Earth (1-5). Here we ask: How does cellular metabolic evolution shape the mass and energy flows of ecosystems? The oceanic phytoplankter Prochlorococcus (6), the most abundant photosynthetic cell on Earth (7,8), provides an ideal model system for addressing this question. Prochlorococcus and its deeper-branching sister lineage marine Synechococcus make up the marine picocyanobacteria and have a characteristic biogeography (9). Prochlorococcus "ecotypes" have geographically (10, 11) and seasonally (12) dynamic populations that in warm, stable stratified water columns always return to the same general structure: Recently diverging highlight-adapted (HL) ecotypes are most abundant toward the surface, whereas deeper branching low-light-adapted (LL) ecotypes are most abundant at depth (10-14) (Fig. 1).What selective forces drove this niche partitioning in Prochlorococcus, and what were the consequences for the ocean ecosystem in general? To address these questions, we reconstructed (15, 16) (Fig. 2) the evolution of core metabolism in strains representing the major clades of Prochlorococcus. To interpret the observed patterns, we developed an evolutionary framework that illuminates the driving forces that produc...

Competitive inhibition of cobalt uptake by zinc and manganese in a pacificProchlorococcusstrain: Insights into metal homeostasis in a streamlined oligotrophic cyanobacterium

“…Recent molecular clock analyses have suggested that genome streamlining in Prochlorococcus occurred during the Neoproterozoic (500–1000 MYA), well after the Great Oxidation Event of ∼ 2.4 billion years ago, followed by the further differentiation of modern Prochlorococcus ecotypes during the Phanerozoic. (Sánchez‐Baracaldo ; Braakman et al ). Despite rising atmospheric O 2 levels during this time, the oceans were not uniformly oxygenated (Sperling et al ), which probably maintained large cobalt sources from anoxic sediments, as observed in the modern ocean (Hawco et al ).…”

“…Cultures growing at high Ni 0 held higher Ni quotas and experienced longer lag phases prior to exponential growth. While it is difficult to evaluate if higher Ni quotas reflect increases in intracellular or periplasmic Ni, the cbiK cobaltochelatase enzyme also has a strong affinity for Ni and is used by some organisms in the biosynthesis of the Ni containing tetrapyrrole F430 (Brindley et al 2003;Moore et al 2017). It is possible that this long lag phase is needed to upregulate Nibinding proteins to decrease competition with cobalt at the binding site of cbiK.…”

Cross‐protection from hydrogen peroxide by helper microbes: the impacts on the cyanobacterium Prochlorococcus and other beneficiaries in marine communities

“…DOM can exit microbial cells and enter the DOM pool in several ways: sloppy feeding by grazers, lysis by virus, 'spontaneous' (i.e., abiotic-induced) cell lysis, excretion from live cells, and release of membrane vesicles (Nagata and Kirchman, 1991;Ankrah et al, 2014;Biller et al, 2014). Studies thus far indicate that Prochlorococcus can release significant amounts of DOM via excretion and vesicle formation (Bertilsson et al, 2005;Becker et al, 2014;Biller et al, 2014;Braakman et al, 2017), and this release may constitute a significant return on the investment for the HOOH-consuming heterotrophic bacteria. Studies thus far indicate that Prochlorococcus can release significant amounts of DOM via excretion and vesicle formation (Bertilsson et al, 2005;Becker et al, 2014;Biller et al, 2014;Braakman et al, 2017), and this release may constitute a significant return on the investment for the HOOH-consuming heterotrophic bacteria.…”

Dynamics of Prochlorococcus and Synechococcus at Station ALOHA Revealed through Flow Cytometry and High-Resolution Vertical Sampling

“…If niche selection of genomes adapted to different niches in the water column plays a role, it is most likely to occur in the stable pycnocline where populations remain segregated over longer periods (weeks to month, or longer). Light intensity is not the only, or even the major defining difference between the periodically mixed-layer and the stable pycnocline (Braakman et al, 2017). Compared to the mixed-layer zone, the pycnocline has higher nutrient concentrations with a different composition .…”