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Escherichia coli utilizes multiple peptidoglycan recycling permeases with distinct strategies of recycling
Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, United States.
Umeå universitet, Medicinska fakulteten, Molekylär Infektionsmedicin, Sverige (MIMS). Umeå universitet, Medicinska fakulteten, Umeå Centre for Microbial Research (UCMR). Umeå universitet, Medicinska fakulteten, Institutionen för molekylärbiologi (Medicinska fakulteten).ORCID-id: 0000-0002-6848-5134
Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, United States.
Umeå universitet, Medicinska fakulteten, Molekylär Infektionsmedicin, Sverige (MIMS). Umeå universitet, Medicinska fakulteten, Umeå Centre for Microbial Research (UCMR). Umeå universitet, Medicinska fakulteten, Institutionen för molekylärbiologi (Medicinska fakulteten).ORCID-id: 0000-0001-5995-718x
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2023 (Engelska)Ingår i: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 120, nr 44, artikel-id e2308940120Artikel i tidskrift (Refereegranskat) Published
Abstract [en]

Bacteria produce a structural layer of peptidoglycan (PG) that enforces cell shape, resists turgor pressure, and protects the cell. As bacteria grow and divide, the existing layer of PG is remodeled and PG fragments are released. Enterics such as Escherichia coli go to great lengths to internalize and reutilize PG fragments. E. coli is estimated to break down one-third of its cell wall, yet only loses ~0 to 5% of meso-diaminopimelic acid, a PG-specific amino acid, per generation. Two transporters were identified early on to possibly be the primary permease that facilitates PG fragment recycling, i) AmpG and ii) the Opp ATP binding cassette transporter in conjunction with a PG-specific periplasmic binding protein, MppA. The contribution of each transporter to PG recycling has been debated. Here, we have found that AmpG and MppA/Opp are differentially regulated by carbon source and growth phase. In addition, MppA/Opp is uniquely capable of high-affinity scavenging of muropeptides from growth media, demonstrating that AmpG and MppA/Opp allow for different strategies of recycling PG fragments. Altogether, this work clarifies environmental contexts under which E. coli utilizes distinct permeases for PG recycling and explores how scavenging by MppA/Opp could be beneficial in mixed communities.

Ort, förlag, år, upplaga, sidor
Proceedings of the National Academy of Sciences (PNAS), 2023. Vol. 120, nr 44, artikel-id e2308940120
Nyckelord [en]
AmpG, cell wall, muropeptides, peptidoglycan, peptidoglycan recycling
Nationell ämneskategori
Mikrobiologi
Identifikatorer
URN: urn:nbn:se:umu:diva-216380DOI: 10.1073/pnas.2308940120ISI: 001124085100001PubMedID: 37871219Scopus ID: 2-s2.0-85175497598OAI: oai:DiVA.org:umu-216380DiVA, id: diva2:1811088
Forskningsfinansiär
Vetenskapsrådet, 2018-05882Vetenskapsrådet, 2018-02823Knut och Alice Wallenbergs Stiftelse, KAW2012.0184KempestiftelsernaNIH (National Institutes of Health), AI176776NIH (National Institutes of Health), AI138576NIH (National Institutes of Health), AI150098NIH (National Institutes of Health), F32 GM137554Tillgänglig från: 2023-11-10 Skapad: 2023-11-10 Senast uppdaterad: 2024-03-20Bibliografiskt granskad
Ingår i avhandling
1. Studies on cell wall recycling and modification in Gram-negative bacteria
Öppna denna publikation i ny flik eller fönster >>Studies on cell wall recycling and modification in Gram-negative bacteria
2024 (Engelska)Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
Alternativ titel[sv]
Studier om cellväggsåtervinning och modifiering i gramnegativa bakterier
Abstract [en]

The bacterial cell wall is made from peptidoglycan (PG), a heteropolymer which forms a bag-like exoskeleton that envelopes the cell. PG is constantly remodelled during growth and division, and in response to environmental stimuli. Decades of study of this process have focused largely on a select few model organisms, leaving its diversity poorly understood. In this thesis, I present studies on different aspects of PG recycling and modification in several Gram-negative models, with a particular focus on the plant pathogen Agrobacterium tumefaciens, a model of the Hyphomicrobiales group of the Alphaproteobacteria which includes several species of medical and environmental interest. It is shown that A. tumefaciens encodes a novel PG transporter, which is vital for cell wall integrity and resistance to β- lactam antibiotics, and widely conserved in the Hyphomicrobiales and Rhodobacterales orders. Growth defects caused by the loss of the transporter are suppressed by mutations in a novel glycopolymer, which is hypothesized to play a role in sequestering metal ions and thereby lowering periplasmic oxidative stress. Next, in collaboration, it is shown that PG recycling in the best studied model, Escherichia coli, is more complicated than previously thought. Rather than depending mostly on the MFS-family transporter AmpG, E. coli uses an ABC transporter, MppA-OppBCDF or AmpG depending on the growth phase and conditions. Finally, two studies on modification of PG by deacetylation are presented. First, A. tumefaciens is shown to encode a novel anhydroMurNAc deacetylase, which specifically deacetylates the PG chain termini. Then, it is shown that the causative agent of Legionnaires’ disease, Legionella pneumophila, depends on deacetylation of its PG during infection for defence against host lysozyme and correct polar placement of its type IV secretion system. 

Ort, förlag, år, upplaga, sidor
Umeå: Umeå University, 2024. s. 53
Serie
Umeå University medical dissertations, ISSN 0346-6612 ; 2300
Nyckelord
Peptidoglycan recycling, bacterial cell wall, antibiotics, Agrobacterium tumefaciens, Escherichia coli, Legionella pneumophila
Nationell ämneskategori
Mikrobiologi
Forskningsämne
mikrobiologi; biokemi
Identifikatorer
urn:nbn:se:umu:diva-222530 (URN)978-91-8070-295-9 (ISBN)978-91-8070-296-6 (ISBN)
Disputation
2024-04-19, Major Groove, Building 6L, Norrlands Universitetssjukhus, Umeå, 09:00 (Engelska)
Opponent
Handledare
Anmärkning

Number in series missing in publication. 

Tillgänglig från: 2024-03-28 Skapad: 2024-03-20 Senast uppdaterad: 2024-03-21Bibliografiskt granskad

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Gilmore, Michael C.Cava, Felipe

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Molekylär Infektionsmedicin, Sverige (MIMS)Umeå Centre for Microbial Research (UCMR)Institutionen för molekylärbiologi (Medicinska fakulteten)
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Proceedings of the National Academy of Sciences of the United States of America
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