Cultivation-independent surveys have shown that the desert soils of Antarctica harbour surprisingly rich microbial communities 1-3 . Given that phototroph abundance varies across these Antarctic soils 2,4 , an enduring question is what supports life in those communities with low photosynthetic capacity 3,5 . Here we provide evidence that atmospheric trace gases are the primary energy sources of two Antarctic surface soil communities. We reconstructed 23 draft genomes from metagenomic reads, including genomes from the candidate bacterial phyla WPS-2 and AD3. The dominant community members encoded and expressed high-affinity hydrogenases, carbon monoxide dehydrogenases, and a RuBisCO lineage known to support chemosynthetic carbon fixation 6,7 . Soil microcosms aerobically scavenged atmospheric H 2 and CO at rates sufficient to sustain their theoretical maintenance energy and mediated substantial levels of chemosynthetic but not photosynthetic CO 2 fixation. We propose that atmospheric H 2 , CO 2 and CO provide dependable sources of energy and carbon to support these communities, which suggests that atmospheric energy sources can provide an alternative basis for ecosystem function to solar or geological energy sources 8,9 . Although more extensive sampling is required to verify whether this process is widespread in terrestrial Antarctica and other oligotrophic habitats, our results provide new understanding of the minimal nutritional requirements for life and open the possibility that atmospheric gases support life on other planets.Terrestrial Antarctica is among the most extreme environments on Earth. Its inhabitants experience the cumulative stresses of freezing temperatures, limited carbon, nitrogen and water availability, strong UV radiation, and frequent freeze-thaw cycles 2,10,11 . Although it was once believed that these conditions restrict life, we now know that the continent hosts a surprising diversity of macrofauna and microbiota 1,2,12 . Surveys indicate that the phylum-level composition of microbial communities in Antarctic soils is similar to those of temperate soils 3 , but Antarctic communities are highly specialized at the species level and strongly structured by physicochemical factors 1,3,10 . In many Antarctic soils, microorganisms are thought to live in dormant states 2 , with metabolic energy directed towards cell maintenance rather than growth 13 . However, it is unclear how these communities obtain the energy and carbon needed for maintenance, given that these soils are often low in organic carbon and contain few classical primary producers 2,5 .
Significance Populations of larger organisms should be more efficient in their resource use, but grow more slowly, than populations of smaller organisms. The relations between size, metabolism, and demography form the bedrock of metabolic theory, but most empirical tests have been correlative and indirect. Experimental lineages of Escherichia coli that evolved to make larger cells provide a unique opportunity to test how size, metabolism, and demography covary. Despite the larger cells having a relatively slower metabolism, they grow faster than smaller cells. They achieve this growth rate advantage by reducing the relative costs of producing their larger cells. That evolution can decouple the costs of production from size challenges a fundamental assumption about the connections between physiology and ecology.
Body size covaries with population dynamics across lifes domains. Theory holds that metabolism imposes fundamental constraints on the coevolution of size and demography. However, studies of interspecific patterns are confounded by other factors that covary with size and demography, and experimental tests of the causal links remain elusive. Here we leverage a 60,000-generation experiment in which Escherichia coli populations evolved larger cells to examine intraspecific metabolic scaling and correlations with demographic parameters. Metabolic theory successfully predicted the relations among size, metabolism, and maximum population density, with strong support for Damuths law of energy equivalence in this experiment. In contrast, populations of larger cells grew faster than those of smaller cells, contradicting the fundamental assumption that costs of production should increase proportionately with size. The finding that the costs of production are substantially decoupled from size requires re-examining the evolutionary drivers and ecological consequences of biological size more generally.
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