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Engineering archaeal membrane-spanning lipid GDGT biosynthesis in bacteria: Implications for early life membrane transformations

Huahui Chen,Fengfeng Zheng,Xi Feng,Zijing Huang,Wei Yang,Chuanlun Zhang,Wenbin Du,Kira S. Makarova,Eugene V. Koonin,Zhirui Zeng

Eukaryotes are hypothesized to be archaeal–bacterial chimeras. Given the different chemical structures of membrane phospholipids in archaea and bacteria, transformations of membranes during eukaryogenesis that led to the bacterial-type membranes of eukaryotic cells remain a major conundrum. One of the possible intermediates of eukaryogenesis could involve an archaeal–bacterial hybrid membrane. So far, organisms with hybrid membranes have not been discovered, and experimentation on such membranes has been limited. To generate mixed membranes, we reconstructed the archaeal membrane lipid biosynthesis pathway in Escherichia coli , creating three strains that individually produced archaeal lipids ranging from simple, such as DGGGOH (digeranylgeranylglycerol) and archaeol, to complex, such as GDGT (glycerol dialkyl glycerol tetraether). The physiological responses became more pronounced as the hybrid membrane incorporated more complex archaeal membrane lipids. In particular, biosynthesis of GDGT induced a pronounced SOS response, accompanied by cellular filamentation, explosive cell lysis, and ATP accumulation. Thus, bacteria seem to be able to incorporate simple archaeal membrane lipids, such as DGGGOH and archaeol, without major fitness costs, compatible with the involvement of hybrid membranes at the early stages of cell evolution and in eukaryogenesis. By contrast, the acquisition of more complex, structurally diverse membrane lipids, such as GDGT, appears to be strongly deleterious to bacteria, suggesting that this type of lipid is an archaeal innovation. Impact statement The formation of archaeal–bacterial hybrid membranes represents possible intermediates in early life evolution and eukaryogenesis. In this study, we synthesized archaeal membrane-spanning lipid GDGT (glycerol dialkyl glycerol tetraether) in bacteria Escherichia coli to create such hybrid membranes and examined their physiological properties. Our results suggest that the formation of hybrid membranes containing simple archaeal-type lipids could be a plausible intermediate stage at major evolutionary transitions, whereas more complex, membrane-spanning lipid GDGT would have been deleterious and probably represent a later archaeal innovation, possibly an adaption to thermal habitats. These findings provide new insights and perspectives into the evolution of membranes at the earliest stages of cellular evolution as well as at eukaryogenesis.