Microbial biosynthesis of wax esters during desiccation: an adaptation for colonization of the earliest terrestrial environments?

Biology – Quantitative Biology – Genomics

Scientific paper

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0414 Biogeochemical Cycles, Processes, And Modeling (0412, 0793, 1615, 4805, 4912), 0456 Life In Extreme Environments, 0458 Limnology (1845, 4239, 4942), 0465 Microbiology: Ecology, Physiology And Genomics (4840), 1055 Organic And Biogenic Geochemistry

Scientific paper

Biosynthesis of wax esters (WE) by prokaryotes in natural systems, notably bacteria from hot springs and marine phytoplankton, is poorly documented, primarily because saponification is a routine step in the analysis of microbial mat lipids. Use of this preparative procedure, critical for characterization of the diagnostic distributions of carboxylic acids in phospholipids, precludes recovery of intact WE. Examination of non-saponified lipids in emergent and desiccated mats with comparable microbial communities from the Warner Lake region, Oregon, reveals increases in the relative abundance (18.6 to 59.9μg/g Corg) and average chain length (C38 to C46) of WE in the latter, combined with assimilation of phytol and tocopherol moieties. Prokaryotes can accumulate WE as storage lipids in vitro, notably at elevated temperature or under nitrogen limiting conditions, but we propose that biosynthesis of long-chain WE that have a low solubility and are resistant to degradation/oxidation may represent an evolutionary strategy to survive desiccation in evaporative environments. Moreover, aeolian transport of desiccated mat-rip-ups between lake flats allows for migration of microbial communities within and between lake flats and basins during arid conditions. Subsequent rehydration within an alkaline environment would naturally saponify WE, and thereby regenerate alcohol and acid moieties that could serve as membrane lipids for the next viable microbial generation. The evolutionary cradle of WE was likely abiotic generation under hydrothermal conditions, which is consistent with the antiquity of the ester linkage necessitated by its integral role in the membranes of Eubacteria (though not Archaea) and in bacteriochlorophyll. The subsequent capability of microbes to biosynthesize WE may have facilitated their survival when nutrients were limiting, and production of long-chain WE (>C40) may represent a further critical evolutionary threshold that enabled their persistence through and during dehydration or desiccation cycles. Thus, production of WE may have facilitated microbial migration to the lake environments that represented the earliest terrestrial ecosystems, and survival through the Great Oxygenation Event.

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