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Physiological limits to life in anoxic subseafloor sediment.

ABSTRACT: In subseafloor sediment, microbial cell densities exponentially decrease with depth into the fermentation zone. Here, we address the classical question of 'why are cells dying faster than they are growing?' from the standpoint of physiology. The stoichiometries of fermentative ATP production and consumption in the fermentation zone place bounds on the conversion of old cell biomass into new. Most fermentable organic matter in deep subseafloor sediment is amino acids from dead cells because cells are mostly protein by weight. Conversion of carbon from fermented dead cell protein into methanogen protein via hydrogenotrophic and acetoclastic methanogenesis occurs at ratios of ?200:1 and 100:1, respectively, while fermenters can reach conversion ratios approaching 6:1. Amino acid fermentations become thermodynamically more efficient at lower substrate and product concentrations, but the conversion of carbon from dead cell protein into fermenter protein is low because of the high energetic cost of translation. Low carbon conversion factors within subseafloor anaerobic feeding chains account for exponential declines in cellular biomass in the fermentation zone of anoxic sediments. Our analysis points to the existence of a life-death transition zone in which the last biologically catalyzed life processes are replaced with purely chemical reactions no longer coupled to life.

SUBMITTER: Orsi WD

PROVIDER: S-EPMC7269680 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Physiological limits to life in anoxic subseafloor sediment.

Orsi William D WD Schink Bernhard B Buckel Wolfgang W Martin William F WF

FEMS microbiology reviews 20200301 2

In subseafloor sediment, microbial cell densities exponentially decrease with depth into the fermentation zone. Here, we address the classical question of 'why are cells dying faster than they are growing?' from the standpoint of physiology. The stoichiometries of fermentative ATP production and consumption in the fermentation zone place bounds on the conversion of old cell biomass into new. Most fermentable organic matter in deep subseafloor sediment is amino acids from dead cells because cells ...[more]

PMID: 32065239

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Project description:Beneath the seafloor, microbial life subsists in isolation from the surface world under persistent energy limitation. The nature and extent of genomic evolution in subseafloor microbes have been unknown. Here, we show that the genomes of Thalassospira bacterial populations cultured from million-year-old subseafloor sediments evolve in clonal populations by point mutation, with a relatively low rate of homologous recombination and elevated numbers of pseudogenes. Ratios of nonsynonymous to synonymous substitutions correlate with the accumulation of pseudogenes, consistent with a role for genetic drift in the subseafloor strains but not in type strains of Thalassospira isolated from the surface world. Consistent with this, pangenome analysis reveals that the subseafloor bacterial genomes have a significantly lower number of singleton genes than the type strains, indicating a reduction in recent gene acquisitions. Numerous insertion-deletion events and pseudogenes were present in a flagellar operon of the subseafloor bacteria, indicating that motility is nonessential in these million-year-old subseafloor sediments. This genomic evolution in subseafloor clonal populations coincided with a phenotypic difference: all subseafloor isolates have a lower rate of growth under laboratory conditions than the Thalassospira xiamenensis type strain. Our findings demonstrate that the long-term physical isolation of Thalassospira, in the absence of recombination, has resulted in clonal populations whereby reduced access to novel genetic material from neighbors has resulted in the fixation of new mutations that accumulate in genomes over millions of years. IMPORTANCE The nature and extent of genomic evolution in subseafloor microbial populations subsisting for millions of years below the seafloor are unknown. Subseafloor populations have ultralow metabolic rates that are hypothesized to restrict reproduction and, consequently, the spread of new traits. Our findings demonstrate that genomes of cultivated bacterial strains from the genus Thalassospira isolated from million-year-old abyssal sediment exhibit greatly reduced levels of homologous recombination, elevated numbers of pseudogenes, and genome-wide evidence of relaxed purifying selection. These substitutions and pseudogenes are fixed into the population, suggesting that the genome evolution of these bacteria has been dominated by genetic drift. Thus, reduced recombination, stemming from long-term physical isolation, resulted in small clonal populations of Thalassospira that have accumulated mutations in their genomes over millions of years.

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Physiological limits to life in anoxic subseafloor sediment.

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Physiological limits to life in anoxic subseafloor sediment.

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