Calditol-linked membrane lipids are required for acid tolerance in Sulfolobus acidocaldarius

Zhirui Zeng, Xiao-Lei Liu, Jeremy H. Wei, Roger E. Summons, and Paula V. Welander
PNAS December 18, 2018 115 (51) 12932-12937; published ahead of print December 5, 2018 https://doi.org/10.1073/pnas.1814048115

  1. Edited by Katherine H. Freeman, Pennsylvania State University, University Park, PA, and approved November 7, 2018 (received for review August 14, 2018)

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Significance

It is thought that the distinct ether lipid membranes of archaea allow them to thrive in environmental extremes. However, it has been difficult to demonstrate this physiological role directly. Here, we identify a protein required for the biosynthesis of a unique archaeal lipid head group, calditol, whose production was considered to be restricted to a subset of archaeal thermoacidophiles. We show that deletion of this protein in Sulfolobus acidocaldarius prevents production of calditol-linked membrane lipids and, in turn, inhibits cell growth at extremely low pH. Our findings also suggest that archaea more broadly, like bacteria, employ radical S-adenosylmethionine proteins to modify membrane lipids in ways that confer protective effects when environmental conditions, such as pH, fluctuate significantly.

Abstract

Archaea have many unique physiological features of which the lipid composition of their cellular membranes is the most striking. Archaeal ether-linked isoprenoidal membranes can occur as bilayers or monolayers, possess diverse polar head groups, and a multiplicity of ring structures in the isoprenoidal cores. These lipid structures are proposed to provide protection from the extreme temperature, pH, salinity, and nutrient-starved conditions that many archaea inhabit. However, many questions remain regarding the synthesis and physiological role of some of the more complex archaeal lipids. In this study, we identify a radical S-adenosylmethionine (SAM) protein in Sulfolobus acidocaldarius required for the synthesis of a unique cyclopentyl head group, known as calditol. Calditol-linked glycerol dibiphytanyl glycerol tetraethers (GDGTs) are membrane spanning lipids in which calditol is ether bonded to the glycerol backbone and whose production is restricted to a subset of thermoacidophilic archaea of the Sulfolobales order within the Crenarchaeota phylum. Several studies have focused on the enzymatic mechanism for the synthesis of the calditol moiety, but to date no protein that catalyzes this reaction has been discovered. Phylogenetic analyses of this putative calditol synthase (Cds) reveal the genetic potential for calditol–GDGT synthesis in phyla other than the Crenarchaeota, including the Korarchaeota and Marsarchaeota. In addition, we identify Cds homologs in metagenomes predominantly from acidic ecosystems. Finally, we demonstrate that deletion of calditol synthesis renders S. acidocaldarius sensitive to extremely low pH, indicating that calditol plays a critical role in protecting archaeal cells from acidic stress.

Footnotes

  • ↵1Z.Z. and X.-L.L. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: welander{at}stanford.edu.

  • Author contributions: Z.Z., X.-L.L., R.E.S., and P.V.W. designed research; Z.Z., X.-L.L., and P.V.W. performed research; X.-L.L. and J.H.W. contributed new reagents/analytic tools; Z.Z., X.-L.L., J.H.W., R.E.S., and P.V.W. analyzed data; and Z.Z., X.-L.L., J.H.W., R.E.S., and P.V.W. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1814048115/-/DCSupplemental.

Published under the PNAS license.

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Calditol-linked membrane lipids are required for acid tolerance in Sulfolobus acidocaldarius
Zhirui Zeng, Xiao-Lei Liu, Jeremy H. Wei, Roger E. Summons, Paula V. Welander
Proceedings of the National Academy of Sciences Dec 2018, 115 (51) 12932-12937; DOI: 10.1073/pnas.1814048115
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