A bioenergetic basis for membrane divergence in archaea and bacteria.

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...

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Autores principales:	Víctor Sojo, Andrew Pomiankowski, Nick Lane
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/d4c4c2f9d73b49d4927215c427437de7
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spelling	oai:doaj.org-article:d4c4c2f9d73b49d4927215c427437de72021-11-25T05:33:00ZA bioenergetic basis for membrane divergence in archaea and bacteria.1544-91731545-788510.1371/journal.pbio.1001926https://doaj.org/article/d4c4c2f9d73b49d4927215c427437de72014-08-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/25116890/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Membrane 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.Víctor SojoAndrew PomiankowskiNick LanePublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 12, Iss 8, p e1001926 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Víctor Sojo Andrew Pomiankowski Nick Lane A bioenergetic basis for membrane divergence in archaea and bacteria.
description	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.
format	article
author	Víctor Sojo Andrew Pomiankowski Nick Lane
author_facet	Víctor Sojo Andrew Pomiankowski Nick Lane
author_sort	Víctor Sojo
title	A bioenergetic basis for membrane divergence in archaea and bacteria.
title_short	A bioenergetic basis for membrane divergence in archaea and bacteria.
title_full	A bioenergetic basis for membrane divergence in archaea and bacteria.
title_fullStr	A bioenergetic basis for membrane divergence in archaea and bacteria.
title_full_unstemmed	A bioenergetic basis for membrane divergence in archaea and bacteria.
title_sort	bioenergetic basis for membrane divergence in archaea and bacteria.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/d4c4c2f9d73b49d4927215c427437de7
work_keys_str_mv	AT victorsojo abioenergeticbasisformembranedivergenceinarchaeaandbacteria AT andrewpomiankowski abioenergeticbasisformembranedivergenceinarchaeaandbacteria AT nicklane abioenergeticbasisformembranedivergenceinarchaeaandbacteria AT victorsojo bioenergeticbasisformembranedivergenceinarchaeaandbacteria AT andrewpomiankowski bioenergeticbasisformembranedivergenceinarchaeaandbacteria AT nicklane bioenergeticbasisformembranedivergenceinarchaeaandbacteria
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A bioenergetic basis for membrane divergence in archaea and bacteria.

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