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The emergence and early evolution of biological carbon-fixation.

ABSTRACT: The fixation of CO? into living matter sustains all life on Earth, and embeds the biosphere within geochemistry. The six known chemical pathways used by extant organisms for this function are recognized to have overlaps, but their evolution is incompletely understood. Here we reconstruct the complete early evolutionary history of biological carbon-fixation, relating all modern pathways to a single ancestral form. We find that innovations in carbon-fixation were the foundation for most major early divergences in the tree of life. These findings are based on a novel method that fully integrates metabolic and phylogenetic constraints. Comparing gene-profiles across the metabolic cores of deep-branching organisms and requiring that they are capable of synthesizing all their biomass components leads to the surprising conclusion that the most common form for deep-branching autotrophic carbon-fixation combines two disconnected sub-networks, each supplying carbon to distinct biomass components. One of these is a linear folate-based pathway of CO? reduction previously only recognized as a fixation route in the complete Wood-Ljungdahl pathway, but which more generally may exclude the final step of synthesizing acetyl-CoA. Using metabolic constraints we then reconstruct a "phylometabolic" tree with a high degree of parsimony that traces the evolution of complete carbon-fixation pathways, and has a clear structure down to the root. This tree requires few instances of lateral gene transfer or convergence, and instead suggests a simple evolutionary dynamic in which all divergences have primary environmental causes. Energy optimization and oxygen toxicity are the two strongest forces of selection. The root of this tree combines the reductive citric acid cycle and the Wood-Ljungdahl pathway into a single connected network. This linked network lacks the selective optimization of modern fixation pathways but its redundancy leads to a more robust topology, making it more plausible than any modern pathway as a primitive universal ancestral form.

SUBMITTER: Braakman R

PROVIDER: S-EPMC3334880 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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The emergence and early evolution of biological carbon-fixation.

Braakman Rogier R Smith Eric E

PLoS computational biology 20120419 4

The fixation of CO₂ into living matter sustains all life on Earth, and embeds the biosphere within geochemistry. The six known chemical pathways used by extant organisms for this function are recognized to have overlaps, but their evolution is incompletely understood. Here we reconstruct the complete early evolutionary history of biological carbon-fixation, relating all modern pathways to a single ancestral form. We find that innovations in carbon-fixation were the foundation for most major earl ...[more]

PMID: 22536150

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Project description:Macroalgae, commonly known as seaweed, are foundational species in coastal ecosystems and contribute significantly to coastal primary production globally. However, the impact of macroalgal decomposition on benthic biological nitrogen fixation (BNF) after deposition to the seafloor remains largely unexplored. In this study, we measure BNF rates at three different sites at the Big Fisherman's Cove on Santa Catalina Island, CA, USA, which is representative of globally distributed rocky bottom macroalgal habitats. Unamended BNF rates varied among sites (0.001-0.05 nmol N g-1 h -1) and were generally within the lower end of previously reported ranges. We hypothesized that the differences in BNF between sites were linked to the availability of organic matter. Indeed, additions of glucose, a labile carbon source, resulted in 2-3 orders of magnitude stimulation of BNF rates in bottle incubations of sediment from all sites. To assess the impact of complex, autochthonous organic matter, we simulated macroalgal deposition and remineralization with additions of brown (i.e., Macrocystis pyrifera and Dictyopteris), green (i.e., Codium fragile), and red (i.e., Asparagopsis taxiformis) macroalgae. While brown and green macroalgal amendments resulted in 53- to 520-fold stimulation of BNF rates-comparable to the labile carbon addition-red alga was found to significantly inhibit BNF rates. Finally, we employed nifH sequencing to characterize the diazotrophic community associated with macroalgal decomposition. We observed a distinct community shift in potential diazotrophs from primarily Gammaproteobacteria in the early stages of remineralization to a community dominated by Deltaproteobacteria (e.g., sulfate reducers), Bacteroidia, and Spirochaeta toward the latter phase of decomposition of brown, green, and red macroalgae. Notably, the nifH-containing community associated with red macroalgal detritus was distinct from that of brown and green macroalgae. Our study suggests coastal benthic diazotrophs are limited by organic carbon and demonstrates a significant and phylum-specific effect of macroalgal loading on benthic microbial communities.

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The emergence and early evolution of biological carbon-fixation.

Publications

The emergence and early evolution of biological carbon-fixation.

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