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Cited by 19Bacterial Genetics and BiotechnologyLipid Membrane Structure and BehaviorLipid metabolism and biosynthesis

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Genetic evidence for functional diversification of gram-negative intermembrane phospholipid transporters

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Rai, Ashutosh K., Sawasato, Katsuhiro, Bennett, Haley C., Kozlova, Anastasiia, Sparagna, Genevieve C., Bogdanov, Mikhail, Mitchell, Angela M.·2024·PLOS Genetics
DOI 10.1371/journal.pgen.1011335PMC PMC11226057

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Abstract

The outer membrane of gram-negative bacteria is a barrier to chemical and physical stress. Phospholipid transport between the inner and outer membranes has been an area of intense investigation and, in E . coli K-12, it has recently been shown to be mediated by YhdP, TamB, and YdbH, which are suggested to provide hydrophobic channels for phospholipid diffusion, with YhdP and TamB playing the major roles. However, YhdP and TamB have different phenotypes suggesting distinct functions. It remains unclear whether these functions are related to phospholipid metabolism. We investigated a synthetic cold sensitivity caused by deletion of fadR , a transcriptional regulator controlling fatty acid degradation and unsaturated fatty acid production, and yhdP , but not by Δ tamB Δ fadR or Δ ydbH Δ fadR . Deletion of tamB recuses the Δ yhdP Δ fadR cold sensitivity further demonstrating the phenotype is related to functional diversification between these genes. The Δ yhdP Δ fadR strain shows a greater increase in cardiolipin upon transfer to the non-permissive temperature and genetically lowering cardiolipin levels can suppress cold sensitivity. These data also reveal a qualitative difference between cardiolipin synthases in E . coli , as deletion of clsA and clsC suppresses cold sensitivity but deletion of clsB does not. Moreover, increased fatty acid saturation is necessary for cold sensitivity and lowering this level genetically or through supplementation of oleic acid suppresses the cold sensitivity of the Δ yhdP Δ fadR strain. Together, our data clearly demonstrate that the diversification of function between YhdP and TamB is related to phospholipid metabolism. Although indirect regulatory effects are possible, we favor the parsimonious hypothesis that YhdP and TamB have differential phospholipid-substrate transport preferences. Thus, our data provide a potential mechanism for independent control of the phospholipid composition of the inner and outer membranes in response to changing conditions based on regulation of abundance or activity of YhdP and TamB.

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Metadata

Authors
Rai, A. K., Sawasato, K., Bennett, H. C., Kozlova, A., Sparagna, G. C., Bogdanov, M., & Mitchell, A. M.
Affiliations
  • Texas A&M University (US)
  • The University of Texas Health Science Center at Houston (US)
  • University of Colorado Anschutz (US)
Corresponding author
Mitchell, Angela M.
ORCID
Venue
PLOS Genetics
Publisher
Public Library of Science (PLoS)
Published
2024-06-24
Volume
20
Issue
6
Pages
e1011335
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1011335
PMC
PMC11226057
OpenAlex
W4399939543
Cited by
19
References
1
Citations by year
2026: 7 · 2025: 6 · 2024: 5
FWCI
4.76
Type
journal article
Language
en
Update notices
new_version (2024-07-05)
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
  • Digital Commons-TMC (Texas Medical Center) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Division of Microbiology and Infectious Diseases, National Institute of Allergy and Infectious Diseases (R01-AI155915, R01-AI155915-S1)
  • National Institute of General Medical Sciences (R01-GM121493)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
Keywords
phospholipid transport, Gram-negative bacteria, Escherichia coli, cold sensitivity, FadR, cardiolipin, cardiolipin synthase, fatty acid saturation, oleic acid, outer membrane, inner membrane, phospholipid metabolism, functional diversification, membrane lipid composition

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