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Structural insights into Deinococcus radiodurans BamA: extracellular loop diversity and its evolutionary implications

  • 1.

    MOE Key Laboratory for Membraneless Organelles and Cellular Dynamics, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei 230026, China

  • 2.

    College of Life Science, Anhui Agricultural University, Hefei 230036, China

Cite this:
CSTR: 32290.14.JUSTC-2024-0012
https://doi.org/10.52396/JUSTC-2024-0012
More Information
  • Author Bio:

    Zhenzhou Wang is a graduate student at the Division of Life Science and Medicine, University of Science and Technology of China, under the supervision of Prof. Hongwu Qian. His research mainly focuses on the structure and function of important membrane proteins in bacteria

    Jiangliu Yu is currently a Lecturer at Anhui Agricultural University. He received his Ph.D. degree from Zhejiang University under the tutelage of Prof. Bing Tian and Prof. Yuejin Hua in 2017. His research interests include environmental stress resistance of bacteria and bacterial cell structure

    Hongwu Qian is currently a Professor of the Division of Life Science and Medicine, University of Science and Technology of China. He received his B.S. degree from Huazhong University of Science and Technology in 2013 and Ph.D. degree from Tsinghua University in 2018. His research interests include the molecular basis of essential membrane proteins

    Xinxing Yang is currently a Professor of the Division of Life Science and Medicine, University of Science and Technology of China. He received his B.S. degree from Peking University in 2006 and Ph.D. degree from Peking University in 2012. His research interests include the biophysics and cell biology of bacteria

  • Corresponding author: E-mail: 2017074@ahau.edu.cn; E-mail: hongwuqian@ustc.edu.cn; E-mail: xinxingyang@ustc.edu.cn
  • Received Date: 31 January 2024
  • Accepted Date: 08 May 2024
    Abstract

  • Abstract

    Diderm bacteria, characterized by an additional lipid membrane layer known as the outer membrane, fold their outer membrane proteins (OMPs) via the β-barrel assembly machinery (BAM) complex. Understanding how the BAM complex, particularly its key component BamA, assists in OMP folding remains crucial in bacterial cell biology. Recent research has focused primarily on the structural and functional characteristics of BamA within the Gracilicutes clade, such as in Escherichia coli (E. coli). However, another major evolutionary branch, Terrabacteria, has received comparatively less attention. An example of a Terrabacteria is Deinococcus radiodurans (D. radiodurans), a Gram-positive bacterium that possesses a distinctive outer membrane structure. In this study, we first demonstrated that the β-barrel domains of BamA are not interchangeable between D. radiodurans and E. coli. The structure of D. radiodurans BamA was subsequently determined at 3.8 Å resolution using cryo-electron microscopy, revealing obviously distinct arrangements of extracellular loop 4 (ECL4) and ECL6 after structural comparison with their counterparts in gracilicutes. Despite the overall similarity in the topology of the β-barrel domain, our results indicate that certain ECLs have evolved into distinct structures between the Terrabacteria and Gracilicutes clades. While BamA and its function are generally conserved across diderm bacterial species, our findings underscore the evolutionary diversity of this core OMP folder among bacteria, offering new insights into bacterial physiology and evolutionary biology.

    Graphical abstract

    Comparison of the barrel domains of DrBamA and EcBamA (PDB: 5D0O).

    Abstract

    Diderm bacteria, characterized by an additional lipid membrane layer known as the outer membrane, fold their outer membrane proteins (OMPs) via the β-barrel assembly machinery (BAM) complex. Understanding how the BAM complex, particularly its key component BamA, assists in OMP folding remains crucial in bacterial cell biology. Recent research has focused primarily on the structural and functional characteristics of BamA within the Gracilicutes clade, such as in Escherichia coli (E. coli). However, another major evolutionary branch, Terrabacteria, has received comparatively less attention. An example of a Terrabacteria is Deinococcus radiodurans (D. radiodurans), a Gram-positive bacterium that possesses a distinctive outer membrane structure. In this study, we first demonstrated that the β-barrel domains of BamA are not interchangeable between D. radiodurans and E. coli. The structure of D. radiodurans BamA was subsequently determined at 3.8 Å resolution using cryo-electron microscopy, revealing obviously distinct arrangements of extracellular loop 4 (ECL4) and ECL6 after structural comparison with their counterparts in gracilicutes. Despite the overall similarity in the topology of the β-barrel domain, our results indicate that certain ECLs have evolved into distinct structures between the Terrabacteria and Gracilicutes clades. While BamA and its function are generally conserved across diderm bacterial species, our findings underscore the evolutionary diversity of this core OMP folder among bacteria, offering new insights into bacterial physiology and evolutionary biology.

    • Public Summary

    • The β-barrel domain of BamA in Deinococcus radiodurans and Escherichia coli are not interchangeable.
    • The structure of the barrel domain of Deinococcus radiodurans BamA reveals the difference in extracellular loop 4 and 6 compared with that in Escherichia coli BamA.
    • The polar interactions of the helix in extracellular loop 4 with other extracellular loops and the stem region in extracellular loop 6 are important for the function of Escherichia coli BamA.

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    • References(49)
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    Figure  4.  Mapping of ECL4 and ECL6 features on bacterial phylogeny. This figure presents a phylogenetic tree based on Witwinowski et al.[19], collapsed at the phylum level via iTOL v6 (https://itol.embl.de/). It includes one or two BamA structures from each phylum, sourced from previous studies, this research, or AlphaFold2[45] predictions. ECL4 is categorized as either possessing an outer helix or not, with those containing an outer helix further classified on the basis of polar interactions with other extracellular loops. ECL6 classification hinges on the presence of a stem region. The detailed species names and corresponding UniProt accession numbers are available in Table S3.

    Figure  1.  Chimeric EcBamA carrying the β-barrel domain of DrBamA cannot rescue the loss of native EcBamA. (a) Comparison of the barrel domain of BamA orthologs from several gamma- and beta-proteobacteria. Ec: E. coli, St: Salmonella enterica serovar Typhimurium, Hi: Haemophilus influenzae, Pm: Pasteurella multocida, Pa: Pseudomonas aeruginosa, Nm: Neisseria meningitidis. The structures of the barrel domains of EcBamA (PDB code: 5D0O)[8] and StBamA (PDB code: 5OR1)[46] were obtained from RSCB PDB[43, 44], and the others were obtained from the AlphaFold Protein Structure Database[45]. (b) Sequence alignment of the barrel domain of BamA orthologs from the species in (a). ECL4 and ECL6 of EcBamA were labeled. (c) Schematic diagram of the BamA depletion strain. (d) Spot assay of full-length DrBamA and the chimera BamA carrying different domains of DrBamA and EcBamA. EV: empty vector. The results are representative of at least three independent experiments. The same applies hereinafter.

    Figure  2.  Overall structure of the DrBamA dimer. (a) Topologic model of the DrBamA barrel domain. β-strands are shown as arrows, and the α-helix is shown as a cylinder. The transmembrane sheets, ECL4 and ECL6, are colored yellow orange, slate and deep purple, respectively. (b) Cryo-EM map of dimeric DrBamA with each protomer in individual colors. (c) Cartoon representation of the DrBamA dimer from the side view and top view, with one protomer colored rainbow and the other colored as in (a). (d) Polar interactions between the two protomers of DrBamA. (e) Comparison of the barrel domains of DrBamA and EcBamA (PDB: 5D0O)[8].

    Figure  3.  Analysis of ECL4 and ECL6 in BamA. (a, b) Structural alignments of ECL4s (a) and ECL6s (b) in BamA orthologs from different species. The ECL4 and ECL6 products from the proteobacteria were obtained and colored the same as those in Fig. 1(a). The “hairpin-like” topological organization of EcECL6 is shown in addition to the comparison of the ECL6s. (c) Spot assays in which the chimera EcBamA replaced ECL4 or ECL6 with the corresponding region of DrBamA. (d) Overall structure of the EcBamA barrel domain in the intermediate-open state (PDB: 7TT6) [11]. (e) Polar interactions between residues in the outer helix with other extracellular loops in EcBamA. (f) Spot assays of mutants in the outer helix of EcBamA. (g) Hydrogen bonds of the residues in the stem region of EcECL6. (h) Spot assays of different truncated versions of ECL6 in EcBamA. Each region was deleted by replacement with a GS linker (GSGS for “del 670–706” and GSG for “del 676–699”).

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    Tomasek D, Kahne D. The assembly of β-barrel outer membrane proteins. Current Opinion in Microbiology, 2021, 60: 16–23. doi: 10.1016/j.mib.2021.01.009
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    Webb C T, Heinz E, Lithgow T. Evolution of the β-barrel assembly machinery. Trends in Microbiology, 2012, 20 (12): 612–620. doi: 10.1016/j.tim.2012.08.006
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    [5]
    Kaur H, Jakob R P, Marzinek J K, et al. The antibiotic darobactin mimics a β-strand to inhibit outer membrane insertase. Nature, 2021, 593: 125–129. doi: 10.1038/s41586-021-03455-w
    [6]
    Noinaj N, Gumbart J C, Buchanan S K. The β-barrel assembly machinery in motion. Nature Reviews Microbiology, 2017, 15: 197–204. doi: 10.1038/nrmicro.2016.191
    [7]
    Anwari K, Webb C T, Poggio S, et al. The evolution of new lipoprotein subunits of the bacterial outer membrane BAM complex. Molecular Microbiology, 2012, 84 (5): 832–844. doi: 10.1111/j.1365-2958.2012.08059.x
    [8]
    Gu Y, Li H, Dong H, et al. Structural basis of outer membrane protein insertion by the BAM complex. Nature, 2016, 531: 64–69. doi: 10.1038/nature17199
    [9]
    Tomasek D, Rawson S, Lee J, et al. Structure of a nascent membrane protein as it folds on the BAM complex. Nature, 2020, 583: 473–478. doi: 10.1038/s41586-020-2370-1
    [10]
    Wu R, Bakelar J W, Lundquist K, et al. Plasticity within the barrel domain of BamA mediates a hybrid-barrel mechanism by BAM. Nature Communications, 2021, 12: 7131. doi: 10.1038/s41467-021-27449-4
    [11]
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    [12]
    Shen C R, Chang S H, Luo Q H, et al. Structural basis of BAM-mediated outer membrane beta-barrel protein assembly. Nature, 2023, 617: 185–193. doi: 10.1038/s41586-023-05988-8
    [13]
    Arnold T, Zeth K, Linke D. Omp85 from the thermophilic cyanobacterium Thermosynechococcus elongatus differs from proteobacterial Omp85 in structure and domain composition. The Journal of Biological Chemistry, 2010, 285 (23): 18003–18015. doi: 10.1074/jbc.M110.112516
    [14]
    Koenig P, Mirus O, Haarmann R, et al. Conserved properties of polypeptide transport-associated (POTRA) domains derived from cyanobacterial Omp85. Journal of Biological Chemistry, 2010, 285 (23): 18016–18024. doi: 10.1074/jbc.M110.112649
    [15]
    Gatsos X, Perry A J, Anwari K, et al. Protein secretion and outer membrane assembly in Alphaproteobacteria. FEMS Microbiology Reviews, 2008, 32 (6): 995–1009. doi: 10.1111/j.1574-6976.2008.00130.x
    [16]
    Estrada Mallarino L, Fan E, Odermatt M, et al. TtOmp85, a β-barrel assembly protein, functions by barrel augmentation. Biochemistry, 2015, 54 (3): 844–852. doi: 10.1021/bi5011305
    [17]
    Volokhina E B, Grijpstra J, Beckers F, et al. Species-specificity of the BamA component of the bacterial outer membrane protein-assembly machinery. PLoS One, 2013, 8 (12): e85799. doi: 10.1371/journal.pone.0085799
    [18]
    Browning D F, Bavro V N, Mason J L, et al. Cross-species chimeras reveal BamA POTRA and β-barrel domains must be fine-tuned for efficient OMP insertion. Molecular Microbiology, 2015, 97 (4): 646–659. doi: 10.1111/mmi.13052
    [19]
    Witwinowski J, Sartori-Rupp A, Taib N, et al. An ancient divide in outer membrane tethering systems in bacteria suggests a mechanism for the diderm-to-monoderm transition. Nature Microbiology, 2022, 7 (3): 411–422. doi: 10.1038/s41564-022-01066-3
    [20]
    Sexton D L, Burgold S, Schertel A, et al. Super-resolution confocal cryo-CLEM with cryo-FIB milling for in situ imaging of Deinococcus radiodurans. Current Research in Structural Biology, 2022, 4: 1–9. doi: 10.1016/j.crstbi.2021.12.001
    [21]
    Yu J L, Lu L C. BamA is a pivotal protein in cell envelope synthesis and cell division in Deinococcus radiodurans. Biochimica et Biophysica Acta (BBA) - Biomembranes, 2019, 1861 (7): 1365–1374. doi: 10.1016/j.bbamem.2019.05.010
    [22]
    Chen J C, Li Y, Zhang K, et al. Whole-genome sequence of phage-resistant strain Escherichia coli DH5α . Genome Announcements, 2018, 6 (10): e00097–18. doi: 10.1128/genomea.00097-18
    [23]
    Wood W B. Host specificity of DNA produced by Escherichia coli: Bacterial mutations affecting the restriction and modification of DNA . Journal of Molecular Biology, 1966, 16 (1): 118–133. doi: 10.1016/S0022-2836(66)80267-X
    [24]
    Baba T, Ara T, Hasegawa M, et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Molecular Systems Biology, 2006, 2: 2006.0008. doi: 10.1038/msb4100050
    [25]
    Silhavy T J, Berman M L, Enquist L W. Experiments With Gene Fusions. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1984 .
    [26]
    White O, Eisen J A, Heidelberg J F, et al. Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1 . Science, 1999, 286 (5444): 1571–1577. doi: 10.1126/science.286.5444.1571
    [27]
    Anand A, LeDoyt M, Karanian C, et al. Bipartite topology of Treponema pallidum repeat proteins C/D and I: outer membrane insertion, trimerization, and porin function require a C-terminal β-barrel domain . The Journal of Biological Chemistry, 2015, 290 (19): 12313–12331. doi: 10.1074/jbc.M114.629188
    [28]
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    [29]
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