New insights into the role of phosphate-free lipids in anaerobic environments

Recent investigations have revealed an abundance of phosphate-free glycolipids and aminolipids, classically assigned to oxygenic phototrophs, in anoxic environments where anaerobic microorganisms prevail. Phosphorus-free lipids in oxic environments are thought to indicate an adaptation to phosphorus limitation, but their significance in anoxic environments is unclear, because these environments are not typically thought of as phosphorus-limited. We hypothesize that glycolipids and aminolipids play an overlooked and potentially integral role in anaerobic bacteria from marine and terrestrial environments and test this hypothesis in environmentally relevant model anaerobic deltaproteobacteria. None of the investigated strains of the sulfate-reducing genus Desulfovibrio synthesize glycolipids under normal growth conditions or during nitrogen limitation. However, when growing in phosphate-limited conditions, all investigated organisms undergo a nearly complete replacement of phospholipids by glycolipids. Some phosphate-starved organisms, such as D. fructosivorans, are also able to synthesize betaine lipids. Analyses of mutants of Desulfovibrio alaskensis G20 identify genes responsible for the biosynthesis of aminolipids (Dde_3661) and glycolipids (Dde_3613). Fitness experiments using tagged transposon mutant libraries of G20 identify these two genes and 90 other genes important for fitness of this organism during phosphate limitation. These experiments identify for the first time betaine lipids and glycolipids in sulfate-reducing bacteria and demonstrate the importance of these non-phosphorus lipids as substitute lipids in obligate anaerobes. These findings suggest that phosphorus availability limits microbial growth and activity in a more widespread range of environments than previously thought.