Abstract
Sediment-hosted CO2-rich aquifers deep below the Colorado Plateau (USA) contain a remarkable diversity of uncultivated microorganisms, including Candidate Phyla Radiation (CPR) bacteria that are putative symbionts unable to synthesize membrane lipids. The origin of organic carbon in these ecosystems is unknown and the source of CPR membrane lipids remains elusive. We collected cells from deep groundwater brought to the surface by eruptions of Crystal Geyser, sequenced the community, and analyzed the whole community lipidome over time. Characteristic stable carbon isotopic compositions of microbial lipids suggest that bacterial and archaeal CO2 fixation ongoing in the deep subsurface provides organic carbon for the complex communities that reside there. Coupled lipidomic-metagenomic analysis indicates that CPR bacteria lack complete lipid biosynthesis pathways but still possess regular lipid membranes. These lipids may therefore originate from other community members, which also adapt to high in situ pressure by increasing fatty acid unsaturation. An unusually high abundance of lysolipids attributed to CPR bacteria may represent an adaptation to membrane curvature stress induced by their small cell sizes. Our findings provide new insights into the carbon cycle in the deep subsurface and suggest the redistribution of lipids into putative symbionts within this community.
Highlights
Based on existing annotations target proteins involved in bacterial fatty acid (FA), isoprenoids, and lipids biosynthesis were identified in Candidate Phyla Radiation (CPR) genomes and can be accessed using the following link: https://ggkbase. berkeley.edu/genome_summaries/1491-Bacterial_membra ne_lipids_AJP
The red dashed line indicates the relative contribution of autotrophy versus heterotrophy to archaeal lipid biomass, calculated from mass balance of δ13C values of bacterial and archaeal lipids. c Relative abundance of unsaturated diacylglycerol membrane lipids
We found that the CPR genomes do not encode for any known, complete bacterial lipid biosynthesis pathway, yet CPR bacteria are known to have a cytoplasmic membrane based on cryogenic-transmission electron microscopy studies [14]
Summary
Other subsurface environments have low availability of buried organic matter In such environments, genomic analyses suggest that in situ CO2 fixation supports microbial communities [6,7,8,9,10,11]. It was shown that archaea growing in syntrophy with sulfate-reducing bacteria mediate the anaerobic oxidation of methane [21, 22] This analysis was possible because the consortia were based on simple bacterial and archaeal assemblages that produce diagnostic lipid types. A recent large-scale environmental genomics survey of subsurface microbial ecosystems within the Colorado Plateau, USA, provided evidence for a depth-based distribution of organisms affiliated with more than 100 different phylum-level lineages [12]. We use coupled metagenomic-lipidomic data sets to test this approach and to resolve the importance of autotrophy as the source of organic carbon in the studied environment
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