A Bioenergetic Basis for Membrane Divergence in Archaea and Bacteria
Víctor Sojo, Andrew Pomiankowski, Nick Lane mail
Published: August 12, 2014DOI: 10.1371/journal.pbio.1001926
Membrane bioenergetics are universal, yet the phospholipid membranes of archaea and bacteria—the deepest branches in the tree of life—are fundamentally different. This deep divergence in membrane chemistry is reflected in other stark differences between the two domains, including ion pumping and DNA replication. We resolve this paradox by considering the energy requirements of the last universal common ancestor (LUCA). We develop a mathematical model based on the premise that LUCA depended on natural proton gradients. Our analysis shows that such gradients can power carbon and energy metabolism, but only in leaky cells with a proton permeability equivalent to fatty acid vesicles. Membranes with lower permeability (equivalent to modern phospholipids) collapse free-energy availability, precluding exploitation of natural gradients. Pumping protons across leaky membranes offers no advantage, even when permeability is decreased 1,000-fold. We hypothesize that a sodium-proton antiporter (SPAP) provided the first step towards modern membranes. SPAP increases the free energy available from natural proton gradients by ~60%, enabling survival in 50-fold lower gradients, thereby facilitating ecological spread and divergence. Critically, SPAP also provides a steadily amplifying advantage to proton pumping as membrane permeability falls, for the first time favoring the evolution of ion-tight phospholipid membranes. The phospholipids of archaea and bacteria incorporate different stereoisomers of glycerol phosphate. We conclude that the enzymes involved took these alternatives by chance in independent populations that had already evolved distinct ion pumps. Our model offers a quantitatively robust explanation for why membrane bioenergetics are universal, yet ion pumps and phospholipid membranes arose later and independently in separate populations. Our findings elucidate the paradox that archaea and bacteria share DNA transcription, ribosomal translation, and ATP synthase, yet differ in equally fundamental traits that depend on the membrane, including DNA replication.
The archaea and bacteria are the deepest branches of the tree of life. The two groups are similar in morphology and share some fundamental biochemistry, including the genetic code, but the differences between them are stark, and rank among the great unsolved problems in biology. The composition of cell membranes and walls is utterly different in the two groups, while the mechanism of DNA replication seems unrelated. We address a specific paradox, giving new insight into this deep evolutionary split: membrane bioenergetics are universal, yet the membranes themselves are not. We resolve this paradox by considering the energetics of a hypothetical last universal common ancestor (LUCA) in geochemically sustained proton gradients. Using a quantitative model, we show that LUCA could have used proton gradients to drive carbon and energy metabolism, but only if the membranes were leaky. This requirement precluded ion pumping and the early evolution of phospholipid membranes. We constrain a pathway leading from LUCA to the deep divergence of archaea and bacteria on the basis of incremental increases in free-energy availability. We support our inferences with comparative biochemistry and phylogenetics, and show why the late evolution of modern membranes forced divergence in other traits such as DNA replication.
Citation: Sojo V, Pomiankowski A, Lane N (2014) A Bioenergetic Basis for Membrane Divergence in Archaea and Bacteria. PLoS Biol 12(8): e1001926. doi:10.1371/journal.pbio.1001926
Academic Editor: David Penny, Massey University, New Zealand
Received: February 26, 2014; Accepted: July 2, 2014; Published: August 12, 2014
Copyright: © 2014 Sojo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: EPSRC PhD studentship (Victor Sojo), Research grants EPSRC (EP/F500351/1, EP/I017909/1) (Andrew Pomiankowski), Leverhulme Trust (RPG-425) Research grant (Nick Lane). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: Ech, energy-converting hydrogenase; LUCA, last universal common ancestor; SPAP, sodium-proton antiporter; ATPase, ATP synthase
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