Uptake of monoaromatic hydrocarbons during biodegradation by FadL channel-mediated lateral diffusion.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
10 12 2020
Historique:
received: 14 05 2020
accepted: 12 11 2020
entrez: 11 12 2020
pubmed: 12 12 2020
medline: 29 12 2020
Statut: epublish

Résumé

In modern societies, biodegradation of hydrophobic pollutants generated by industry is important for environmental and human health. In Gram-negative bacteria, biodegradation depends on facilitated diffusion of the pollutant substrates into the cell, mediated by specialised outer membrane (OM) channels. Here we show, via a combined experimental and computational approach, that the uptake of monoaromatic hydrocarbons such as toluene in Pseudomonas putida F1 (PpF1) occurs via lateral diffusion through FadL channels. Contrary to classical diffusion channels via which polar substrates move directly into the periplasmic space, PpF1 TodX and CymD direct their hydrophobic substrates into the OM via a lateral opening in the channel wall, bypassing the polar barrier formed by the lipopolysaccharide leaflet on the cell surface. Our study suggests that lateral diffusion of hydrophobic molecules is the modus operandi of all FadL channels, with potential implications for diverse areas such as biodegradation, quorum sensing and gut biology.

Identifiants

pubmed: 33303757
doi: 10.1038/s41467-020-20126-y
pii: 10.1038/s41467-020-20126-y
pmc: PMC7728783
doi:

Substances chimiques

Bacterial Proteins 0
Hydrocarbons, Aromatic 0
Benzene J64922108F

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

6331

Subventions

Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/H000658/1
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R01 GM104495
Pays : United States

Références

J Bacteriol. 1997 May;179(10):3171-80
pubmed: 9150211
Sci Rep. 2015 Jul 07;5:11927
pubmed: 26149193
J Bacteriol. 2000 Mar;182(5):1232-42
pubmed: 10671442
PLoS One. 2010 Nov 29;5(11):e15016
pubmed: 21124774
J Biol Chem. 1994 Mar 18;269(11):8022-8
pubmed: 8132524
Mol Gen Genet. 1995 Mar 10;246(5):570-9
pubmed: 7535376
Prostaglandins Leukot Essent Fatty Acids. 2007 Nov-Dec;77(5-6):355-61
pubmed: 18032007
Science. 1981 Jan 9;211(4478):132-8
pubmed: 7444456
Environ Microbiol. 2003 Dec;5(12):1309-27
pubmed: 14641576
Microbiol Mol Biol Rev. 2003 Dec;67(4):593-656
pubmed: 14665678
Biotechnol Bioeng. 2000 Aug 20;69(4):385-400
pubmed: 10862677
J Phys Chem B. 2019 Apr 4;123(13):2824-2832
pubmed: 30839215
J Comput Chem. 2005 Dec;26(16):1701-18
pubmed: 16211538
Eur Biophys J. 2011 Jul;40(7):843-56
pubmed: 21533652
J Mol Graph. 1996 Feb;14(1):33-8, 27-8
pubmed: 8744570
J Biol Chem. 1986 Jan 5;261(1):167-71
pubmed: 3001045
J Bacteriol. 2000 Apr;182(8):2059-67
pubmed: 10735846
J Bacteriol. 1980 Mar;141(3):1047-51
pubmed: 6988400
Chembiochem. 2010 Jul 5;11(10):1339-43
pubmed: 20533493
J Mol Biol. 1993 Dec 5;234(3):779-815
pubmed: 8254673
J Biol Chem. 1984 Jul 10;259(13):8437-43
pubmed: 6376508
Proc Natl Acad Sci U S A. 2011 Jun 21;108(25):10121-6
pubmed: 21593406
IARC Sci Publ. 1988;(85):3-18
pubmed: 3053447
J Bacteriol. 2001 Nov;183(22):6662-6
pubmed: 11673437
Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21
pubmed: 20057044
Curr Opin Struct Biol. 2005 Aug;15(4):401-7
pubmed: 16005205
Nature. 2019 Mar;567(7749):550-553
pubmed: 30894747
J Struct Biol. 1991 Dec;107(3):268-80
pubmed: 1807357
BMC Biotechnol. 2010 Jun 30;10:49
pubmed: 20587073
Proc Natl Acad Sci U S A. 2008 Jun 24;105(25):8601-6
pubmed: 18559855
Biochim Biophys Acta. 1976 Jul 20;441(1):32-7
pubmed: 952984
Proc Natl Acad Sci U S A. 2014 Jul 22;111(29):10702-7
pubmed: 25002473
Science. 2004 Jun 4;304(5676):1506-9
pubmed: 15178802
J Hazard Mater. 2009 Sep 30;169(1-3):1-15
pubmed: 19442441
Appl Environ Microbiol. 2013 Jul;79(13):4149-53
pubmed: 23584769
J Biotechnol. 2018 Sep 10;281:161-167
pubmed: 30016739
Appl Microbiol Biotechnol. 2002 Jul;59(2-3):143-52
pubmed: 12111139
Trends Biotechnol. 2002 Jun;20(6):243-8
pubmed: 12007492
Methods Mol Biol. 2000;143:97-129
pubmed: 11084904
Acta Crystallogr D Biol Crystallogr. 2012 Apr;68(Pt 4):352-67
pubmed: 22505256
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
Nat Protoc. 2006;1(1):153-61
pubmed: 17406227
J Comput Chem. 2010 Aug;31(11):2169-74
pubmed: 20336801
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
J Phys Chem Lett. 2016 Sep 1;7(17):3446-51
pubmed: 27518381
Eur J Biochem. 1975 May;54(1):55-63
pubmed: 1097251
J Phys Chem B. 2011 Nov 17;115(45):13381-8
pubmed: 21970408
Nature. 2009 Mar 19;458(7236):367-70
pubmed: 19182779
Biochim Biophys Acta. 1972 Jul 7;270(3):301-6
pubmed: 4557430
Microbiology (Reading). 2003 Mar;149(Pt 3):795-805
pubmed: 12634347
J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658-674
pubmed: 19461840
Appl Environ Microbiol. 2008 Dec;74(23):7422-6
pubmed: 18849445
J Chem Phys. 2007 Jan 7;126(1):014101
pubmed: 17212484
Acta Crystallogr D Struct Biol. 2018 Feb 1;74(Pt 2):85-97
pubmed: 29533234
Nature. 2017 Nov 15;551(7680):313-320
pubmed: 29144467
Acta Crystallogr D Biol Crystallogr. 2013 Jul;69(Pt 7):1260-73
pubmed: 23793152

Auteurs

Kamolrat Somboon (K)

School of Chemistry, University of Southampton, Southampton, SO17 1BJ, UK.

Anne Doble (A)

Biosciences Institute, The Medical School, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK.

David Bulmer (D)

Biosciences Institute, The Medical School, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK.

Arnaud Baslé (A)

Biosciences Institute, The Medical School, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK.

Syma Khalid (S)

School of Chemistry, University of Southampton, Southampton, SO17 1BJ, UK. s.khalid@soton.ac.uk.

Bert van den Berg (B)

Biosciences Institute, The Medical School, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK. bert.van-den-berg@ncl.ac.uk.

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Classifications MeSH