The evolution of new lipoprotein subunits of the bacterial outer membrane BAM complex

Khatira Anwari, Chaille T Webb, Sebastian Poggio, Andrew J Perry, Matthew J Belousoff, Nemin Celik, Georg Ramm, Andrew Lovering, R Elizabeth Sockett, John Smit, Christine Jacobs-Wagner, Trevor J Lithgow

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Abstract

The beta-barrel assembly machine (BAM) complex is an essential feature of all bacteria with an outer membrane. The core subunit of the BAM complex is BamA and, in Escherichia coli, four lipoprotein subunits: BamB, BamC, BamD and BamE, also function in the BAM complex. Hidden Markov model analysis was used to comprehensively assess the distribution of subunits of the BAM lipoproteins across all subclasses of proteobacteria. A patchwork distribution was detected which is readily reconciled with the evolution of the alpha-, beta-, gamma-, delta- and epsilon-proteobacteria. Our findings lead to a proposal that the ancestral BAM complex was composed of two subunits: BamA and BamD, and that BamB, BamC and BamE evolved later in a distinct sequence of events. Furthermore, in some lineages novel lipoproteins have evolved instead of the lipoproteins found in E. coli. As an example of this concept, we show that no known species of alpha-proteobacteria has a homologue of BamC. However, purification of the BAM complex from the model alpha-proteobacterium Caulobacter crescentus identified a novel subunit we refer to as BamF, which has a conserved sequence motif related to sequences found in BamC. BamF and BamD can be eluted from the BAM complex under similar conditions, mirroring the BamC:D module seen in the BAM complex of gamma-proteobacteria such as E. coli.
Original languageEnglish
Pages (from-to)832 - 844
Number of pages13
JournalMolecular Microbiology
Volume84
Issue number5
DOIs
Publication statusPublished - 2012

Cite this

Anwari, Khatira ; Webb, Chaille T ; Poggio, Sebastian ; Perry, Andrew J ; Belousoff, Matthew J ; Celik, Nemin ; Ramm, Georg ; Lovering, Andrew ; Sockett, R Elizabeth ; Smit, John ; Jacobs-Wagner, Christine ; Lithgow, Trevor J. / The evolution of new lipoprotein subunits of the bacterial outer membrane BAM complex. In: Molecular Microbiology. 2012 ; Vol. 84, No. 5. pp. 832 - 844.
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abstract = "The beta-barrel assembly machine (BAM) complex is an essential feature of all bacteria with an outer membrane. The core subunit of the BAM complex is BamA and, in Escherichia coli, four lipoprotein subunits: BamB, BamC, BamD and BamE, also function in the BAM complex. Hidden Markov model analysis was used to comprehensively assess the distribution of subunits of the BAM lipoproteins across all subclasses of proteobacteria. A patchwork distribution was detected which is readily reconciled with the evolution of the alpha-, beta-, gamma-, delta- and epsilon-proteobacteria. Our findings lead to a proposal that the ancestral BAM complex was composed of two subunits: BamA and BamD, and that BamB, BamC and BamE evolved later in a distinct sequence of events. Furthermore, in some lineages novel lipoproteins have evolved instead of the lipoproteins found in E. coli. As an example of this concept, we show that no known species of alpha-proteobacteria has a homologue of BamC. However, purification of the BAM complex from the model alpha-proteobacterium Caulobacter crescentus identified a novel subunit we refer to as BamF, which has a conserved sequence motif related to sequences found in BamC. BamF and BamD can be eluted from the BAM complex under similar conditions, mirroring the BamC:D module seen in the BAM complex of gamma-proteobacteria such as E. coli.",
author = "Khatira Anwari and Webb, {Chaille T} and Sebastian Poggio and Perry, {Andrew J} and Belousoff, {Matthew J} and Nemin Celik and Georg Ramm and Andrew Lovering and Sockett, {R Elizabeth} and John Smit and Christine Jacobs-Wagner and Lithgow, {Trevor J}",
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Anwari, K, Webb, CT, Poggio, S, Perry, AJ, Belousoff, MJ, Celik, N, Ramm, G, Lovering, A, Sockett, RE, Smit, J, Jacobs-Wagner, C & Lithgow, TJ 2012, 'The evolution of new lipoprotein subunits of the bacterial outer membrane BAM complex', Molecular Microbiology, vol. 84, no. 5, pp. 832 - 844. https://doi.org/10.1111/j.1365-2958.2012.08059.x

The evolution of new lipoprotein subunits of the bacterial outer membrane BAM complex. / Anwari, Khatira; Webb, Chaille T; Poggio, Sebastian; Perry, Andrew J; Belousoff, Matthew J; Celik, Nemin; Ramm, Georg; Lovering, Andrew; Sockett, R Elizabeth; Smit, John; Jacobs-Wagner, Christine; Lithgow, Trevor J.

In: Molecular Microbiology, Vol. 84, No. 5, 2012, p. 832 - 844.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - The evolution of new lipoprotein subunits of the bacterial outer membrane BAM complex

AU - Anwari, Khatira

AU - Webb, Chaille T

AU - Poggio, Sebastian

AU - Perry, Andrew J

AU - Belousoff, Matthew J

AU - Celik, Nemin

AU - Ramm, Georg

AU - Lovering, Andrew

AU - Sockett, R Elizabeth

AU - Smit, John

AU - Jacobs-Wagner, Christine

AU - Lithgow, Trevor J

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N2 - The beta-barrel assembly machine (BAM) complex is an essential feature of all bacteria with an outer membrane. The core subunit of the BAM complex is BamA and, in Escherichia coli, four lipoprotein subunits: BamB, BamC, BamD and BamE, also function in the BAM complex. Hidden Markov model analysis was used to comprehensively assess the distribution of subunits of the BAM lipoproteins across all subclasses of proteobacteria. A patchwork distribution was detected which is readily reconciled with the evolution of the alpha-, beta-, gamma-, delta- and epsilon-proteobacteria. Our findings lead to a proposal that the ancestral BAM complex was composed of two subunits: BamA and BamD, and that BamB, BamC and BamE evolved later in a distinct sequence of events. Furthermore, in some lineages novel lipoproteins have evolved instead of the lipoproteins found in E. coli. As an example of this concept, we show that no known species of alpha-proteobacteria has a homologue of BamC. However, purification of the BAM complex from the model alpha-proteobacterium Caulobacter crescentus identified a novel subunit we refer to as BamF, which has a conserved sequence motif related to sequences found in BamC. BamF and BamD can be eluted from the BAM complex under similar conditions, mirroring the BamC:D module seen in the BAM complex of gamma-proteobacteria such as E. coli.

AB - The beta-barrel assembly machine (BAM) complex is an essential feature of all bacteria with an outer membrane. The core subunit of the BAM complex is BamA and, in Escherichia coli, four lipoprotein subunits: BamB, BamC, BamD and BamE, also function in the BAM complex. Hidden Markov model analysis was used to comprehensively assess the distribution of subunits of the BAM lipoproteins across all subclasses of proteobacteria. A patchwork distribution was detected which is readily reconciled with the evolution of the alpha-, beta-, gamma-, delta- and epsilon-proteobacteria. Our findings lead to a proposal that the ancestral BAM complex was composed of two subunits: BamA and BamD, and that BamB, BamC and BamE evolved later in a distinct sequence of events. Furthermore, in some lineages novel lipoproteins have evolved instead of the lipoproteins found in E. coli. As an example of this concept, we show that no known species of alpha-proteobacteria has a homologue of BamC. However, purification of the BAM complex from the model alpha-proteobacterium Caulobacter crescentus identified a novel subunit we refer to as BamF, which has a conserved sequence motif related to sequences found in BamC. BamF and BamD can be eluted from the BAM complex under similar conditions, mirroring the BamC:D module seen in the BAM complex of gamma-proteobacteria such as E. coli.

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