Leptospira interrogans encodes a canonical BamA and three novel noNterm Omp85 outer membrane protein paralogs

Adler, B. & de la Pena Moctezuma, A. Leptospira and leptospirosis. Vet. Microbiol. 140, 287–296 (2010).Article 
CAS 
PubMed 

Google Scholar 
Ko, A. I., Goarant, C. & Picardeau, M. Leptospira: The dawn of the molecular genetics era for an emerging zoonotic pathogen. Nat. Rev. 7, 736 (2009).CAS 

Google Scholar 
Costa, F. et al. Global morbidity and mortality of leptospirosis: A systematic review. PLoS Negl. Trop. Dis. 9, e0003898 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Bierque, E., Thibeaux, R., Girault, D., Soupe-Gilbert, M. E. & Goarant, C. A systematic review of Leptospira in water and soil environments. PLoS One 15, e0227055 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Mwachui, M. A., Crump, L., Hartskeerl, R., Zinsstag, J. & Hattendorf, J. Environmental and behavioural determinants of leptospirosis transmission: A systematic review. PLoS Negl. Trop. Dis. 9, e0003843 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Cordonin, C. et al. Pathogenic Leptospira and their animal reservoirs: Testing host specificity through experimental infection. Sci. Rep. 10, 7239 (2020).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Athanazio, D. A. et al. Rattus norvegicus as a model for persistent renal colonization by pathogenic Leptospira interrogans. Acta Trop. 105, 176–180 (2008).Article 
PubMed 

Google Scholar 
Bonilla-Santiago, R. & Nally, J. E. Rat model of chronic leptospirosis. Curr. Protoc. Microbiol. https://doi.org/10.1002/9780471729259.mc12e03s20 (2011).Article 
PubMed 

Google Scholar 
Grassmann, A. A., McBride, A. J., Nally, J. E. & Caimano, M. J. Generation of mammalian host-adapted Leptospira interrogans by cultivation in peritoneal dialysis membrane chamber implantation in rats. Bio-protocol https://doi.org/10.21769/BioProtoc.1536 (2015).Article 
PubMed 

Google Scholar 
Surdel, M. C., Anderson, P. N., Hahn, B. L. & Coburn, J. Hematogenous dissemination of pathogenic and non-pathogenic Leptospira in a short-term murine model of infection. Front. Cell Infect. Microbiol. 12, 917962 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Monahan, A. M., Callanan, J. J. & Nally, J. E. Review paper: Host-pathogen interactions in the kidney during chronic leptospirosis. Vet. Pathol. 46, 792–799 (2009).Article 
CAS 
PubMed 

Google Scholar 
Richer, L., Potula, H. H., Melo, R., Vieira, A. & Gomes-Solecki, M. Mouse model for sublethal Leptospira interrogans infection. Infect. Immun. 83, 4693–4700 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Barragan, V., Nieto, N., Keim, P. & Pearson, T. Meta-analysis to estimate the load of Leptospira excreted in urine: Beyond rats as important sources of transmission in low-income rural communities. BMC Res. Notes 10, 71 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Grassmann, A. A. et al. The FUR-like regulators PerRA and PerRB integrate a complex regulatory network that promotes mammalian host-adaptation and virulence of Leptospira interrogans. PLoS Pathog. 17, e1009078 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Haake, D. A. & Levett, P. N. Leptospirosis in humans. Curr. Top. Microbiol. Immunol. 387, 65–97 (2015).CAS 
PubMed 
PubMed Central 

Google Scholar 
Rajaonarivelo, J. A. et al. Clinical manifestations of human leptospirosis: bacteria matter. Front. Cell Infect. Microbiol. 13, 1259599 (2023).Article 
PubMed 
PubMed Central 

Google Scholar 
Fouts, D. E. et al. What makes a bacterial species pathogenic?: Comparative genomic analysis of the genus Leptospira. PLoS Negl. Trop. Dis. 10, e0004403 (2016).Article 
PubMed 
PubMed Central 

Google Scholar 
Picardeau, M. Virulence of the zoonotic agent of leptospirosis: Still terra incognita?. Nat. Rev. Microbiol. 15, 297–307 (2017).Article 
CAS 
PubMed 

Google Scholar 
Monahan, A. M., Callanan, J. J. & Nally, J. E. Proteomic analysis of Leptospira interrogans shed in urine of chronically infected hosts. Infect. Immun. 76, 4952–4958 (2008).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Caimano, M. J. et al. A model system for studying the transcriptomic and physiological changes associated with mammalian host-adaptation by Leptospira interrogans serovar Copenhageni. PLoS Pathog. 10, e1004004 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Nally, J. E. et al. Pathogenic leptospires modulate protein expression and post-translational modifications in response to mammalian host signals. Front. Cell Infect. Microbiol. 7, 362 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Putz, E. J. et al. Proteomic profiles of Leptospira borgpetersenii serovar Hardjo strains JB197 and HB203 cultured at different temperatures. J Proteomics 295, 105106 (2024).Article 
CAS 
PubMed 

Google Scholar 
Zavala-Alvarado, C. et al. The transcriptional response of pathogenic Leptospira to peroxide reveals new defenses against infection-related oxidative stress. PLoS Pathog. 16, e1008904 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Zavala-Alvarado, C. et al. The oxidative stress response of pathogenic Leptospira is controlled by two peroxide stress regulators which putatively cooperate in controlling virulence. PLoS Pathog. 17, e1009087 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Kavela, S. et al. Use of an integrated multi-omics approach to identify molecular mechanisms and critical factors involved in the pathogenesis of Leptospira. Microbiol. Spectr. 11, e0313522 (2023).Article 
PubMed 

Google Scholar 
Murray, G. L. et al. Genome-wide transposon mutagenesis in pathogenic Leptospira species. Infect. Immun. 77, 810–816 (2009).Article 
CAS 
PubMed 

Google Scholar 
Fernandes, L. G. V., Hornsby, R. L., Nascimento, A. & Nally, J. E. Genetic manipulation of pathogenic Leptospira: CRISPR interference (CRISPRi)-mediated gene silencing and rapid mutant recovery at 37C. Sci. Rep. 11, 1768 (2021).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Yanagihara, Y. et al. Leptospira is an environmental bacterium that grows in waterlogged soil. Microbiol. Spectr. 10, e0215721 (2022).Article 
PubMed 

Google Scholar 
Fraser, C. M. et al. Genomic sequence of a Lyme disease spirochaete Borrelia burgdorferi. Nature 390, 580–586 (1997).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Seshadri, R. et al. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc. Natl. Acad. Sci. U S A 101, 5646–5651 (2004).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Cejkova, D. et al. Whole genome sequences of three Treponema pallidum ssp. pertenue strains: Yaws and syphilis treponemes differ in less than 0.2% of the genome sequence. PLoS Negl. Trop. Dis. 6, e1471 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Weinstock, G. M., Hardham, J. M., McLeod, M. P., Sodergren, E. J. & Norris, S. J. The genome of Treponema pallidum: new light on the agent of syphilis. FEMS Microbiol. Rev. 22, 323–332 (1998).Article 
CAS 
PubMed 

Google Scholar 
Galperin, M. Y. & Koonin, E. V. “Conserved hypothetical” proteins: Prioritization of targets for experimental study. Nucleic Acids Res. 32, 5452–5463 (2004).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
da Costa, W. L. O. et al. Functional annotation of hypothetical proteins from the Exiguobacterium antarcticum strain B7 reveals proteins involved in adaptation to extreme environments, including high arsenic resistance. PLoS One 13, e0198965 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
Ijaq, J., Chandra, D., Ray, M. K. & Jagannadham, M. V. Investigating the functional role of hypothetical proteins from an Antarctic bacterium Pseudomonas sp. Lz4W: Emphasis on identifying proteins involved in cold adaptation. Front. Genet. 13, 825269 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Nascimento, A. L. et al. Genome features of Leptospira interrogans serovar Copenhageni. Braz. J. Med. Biol. Res. 37, 459–477 (2004).Article 
CAS 
PubMed 

Google Scholar 
Adhikarla, H. et al. Lvr, a signaling system that controls global gene regulation and virulence in pathogenic Leptospira. Front. Cell Infect. Microbiol. 8, 45 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
Thibeaux, R. et al. Deciphering the unexplored Leptospira diversity from soils uncovers genomic evolution to virulence. Microb. Genom. https://doi.org/10.1099/mgen.0.000144 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
Robbins, G. T. et al. Evaluation of cell binding activities of Leptospira ECM adhesins. PLoS Negl. Trop. Dis. 9, e0003712 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Hu, W. L. et al. The EbpA-RpoN regulatory pathway of the pathogen Leptospira interrogans is essential for survival in the environment. Appl. Environ. Microbiol. 83, e02377 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Evangelista, K. V. et al. Identification of cell-binding adhesins of Leptospira interrogans. PLoS Negl. Trop. Dis. 8, e3215 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Eshghi, A. et al. An extracellular Leptospira interrogans leucine-rich repeat protein binds human E- and VE-cadherins. Cell Microbiol. 21, e12949 (2019).Article 
PubMed 

Google Scholar 
Haake, D. A. et al. Leptospiral outer membrane proteins OmpL1 and LipL41 exhibit synergistic immunoprotection. Infect. Immun. 67, 6572–6582 (1999).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Llanos Salinas, S. P. et al. GspD, the Type II secretion system secretin of Leptospira, protects hamsters against lethal infection with a virulent L. interrogans isolate. Vaccines (Basel) 8, 759 (2020).Article 
PubMed 

Google Scholar 
Maia, M. A. C. et al. Challenges for the development of a universal vaccine against leptospirosis revealed by the evaluation of 22 vaccine candidates. Front. Cell Infect. Microbiol. 12, 940966 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Bettin, E. B. et al. TonB-dependent receptor epitopes expressed in M. bovis BCG induced significant protection in the hamster model of leptospirosis. Appl. Microbiol. Biotechnol. 106, 173–184 (2022).Article 
CAS 
PubMed 

Google Scholar 
Grassmann, A. A. et al. Discovery of novel leptospirosis vaccine candidates using reverse and structural vaccinology. Front. Immunol. 8, 463 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Schuler, E. & Marconi, R. T. The leptospiral general secretory protein D (gspD), a secretin, elicits complement-independent bactericidal antibody against diverse Leptospira species and serovars. Vaccine X 7, 100089 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Fernandes, L. G. V., Teixeira, A. F. & Nascimento, A. Evaluation of Leptospira interrogans knockdown mutants for LipL32, LipL41, LipL21, and OmpL1 proteins. Front. Microbiol. 14, 1199660 (2023).Article 
PubMed 
PubMed Central 

Google Scholar 
Doyle, M. T. & Bernstein, H. D. Function of the Omp85 superfamily of outer membrane protein assembly factors and polypeptide transporters. Annu. Rev. Microbiol. 76, 259–279 (2022).Article 
CAS 
PubMed 

Google Scholar 
Gentle, I., Gabriel, K., Beech, P., Waller, R. & Lithgow, T. The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J. Cell Biol. 164, 19–24 (2004).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Gentle, I. E., Burri, L. & Lithgow, T. Molecular architecture and function of the Omp85 family of proteins. Mol. Microbiol. 58, 1216–1225 (2005).Article 
CAS 
PubMed 

Google Scholar 
Heinz, E. & Lithgow, T. A comprehensive analysis of the Omp85/TpsB protein superfamily structural diversity, taxonomic occurrence, and evolution. Front. Microbiol. 5, 370 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Ma, X. et al. How BamA recruits OMP substrates via poly-POTRAs domain. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 33, 14690–14702 (2019).CAS 

Google Scholar 
Ni, D. et al. Structural and functional analysis of the β-barrel domain of BamA from Escherichia coli. FASEB J. 28, 2677–2685 (2014).Article 
CAS 
PubMed 

Google Scholar 
Noinaj, N., Gumbart, J. C. & Buchanan, S. K. The β-barrel assembly machinery in motion. Nat. Rev. Microbiol. 15, 197–204 (2017).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Noinaj, N., Kuszak, A. J., Balusek, C., Gumbart, J. C. & Buchanan, S. K. Lateral opening and exit pore formation are required for BamA function. Structure 22, 1055–1062 (2014).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Shen, C. et al. Structural basis of BAM-mediated outer membrane β-barrel protein assembly. Nature 617, 185–193 (2023).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Volokhina, E. B., Beckers, F., Tommassen, J. & Bos, M. P. The β-barrel outer membrane protein assembly complex of Neisseria meningitidis. J. Bacteriol. 191, 7074–7085 (2009).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wang, X., Peterson, J. H. & Bernstein, H. D. Bacterial outer membrane proteins are targeted to the BAM complex by two parallel mechanisms. mBio 12, 10 (2021).Article 
CAS 

Google Scholar 
Voulhoux, R., Bos, M. P., Geurtsen, J., Mols, M. & Tommassen, J. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299, 262–265 (2003).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Noinaj, N. et al. Structural insight into the biogenesis of β-barrel membrane proteins. Nature 501, 385–390 (2013).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Jacob-Dubuisson, F., Guerin, J., Baelen, S. & Clantin, B. Two-partner secretion: as simple as it sounds?. Res. Microbiol. 164, 583–595 (2013).Article 
CAS 
PubMed 

Google Scholar 
Mazar, J. & Cotter, P. A. New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol. 15, 508–515 (2007).Article 
CAS 
PubMed 

Google Scholar 
Maier, T. et al. Conserved Omp85 lid-lock structure and substrate recognition in FhaC. Nat. Commun. 6, 7452 (2015).Article 
ADS 
PubMed 

Google Scholar 
Clantin, B. et al. Structure of the membrane protein FhaC: A member of the Omp85-TpsB transporter superfamily. Science 317, 957–961 (2007).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Li, H., Grass, S., Wang, T., Liu, T. & St Geme, J. W. III. Structure of the Haemophilus influenzae HMW1B translocator protein: Evidence for a twin pore. J. Bacteriol. 189, 7497–7502 (2007).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Gruss, F. et al. The structural basis of autotransporter translocation by TamA. Nat. Struct. Mol. Biol. 20, 1318–1320 (2013).Article 
CAS 
PubMed 

Google Scholar 
Diederichs, K. A. et al. Structural insight into mitochondrial β-barrel outer membrane protein biogenesis. Nat. Commun. 11, 3290 (2020).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Sanchez-Pulido, L., Devos, D., Genevrois, S., Vicente, M. & Valencia, A. POTRA: A conserved domain in the FtsQ family and a class of β-barrel outer membrane proteins. Trends Biochem. Sci. 28, 523–526 (2003).Article 
CAS 
PubMed 

Google Scholar 
Hanson, S. E., Doyle, M. T. & Bernstein, H. D. The patatin-like protein PlpD forms novel structurally dynamic homodimers in the Pseudomonas aeruginosa outer membrane. bioRxiv (2023).Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Desrosiers, D. C. et al. TP0326, a Treponema pallidum β-barrel assembly machinery A (BamA) orthologue and rare outer membrane protein. Mol. Microbiol. 80, 1496–1515 (2011).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Luthra, A. et al. A homology model reveals novel structural features and an immunodominant surface loop/opsonic target in the Treponema pallidum BamA ortholog TP_0326. J. Bacteriol. 197, 1906–1920 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Lenhart, T. R. & Akins, D. R. Borrelia burgdorferi locus BB0795 encodes a BamA orthologue required for growth and efficient localization of outer membrane proteins. Mol. Microbiol. 75, 692–709 (2010).Article 
CAS 
PubMed 

Google Scholar 
Levett, P. N., Morey, R. E., Galloway, R., Steigerwalt, A. G. & Ellis, W. A. Reclassification of Leptospira parva Hovind-Hougen et al. 1982 as Turneriella parva gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 55, 1497–1499 (2005).Article 
CAS 
PubMed 

Google Scholar 
Levett, P. N. Systematics of leptospiraceae. Curr. Top. Microbiol. Immunol. 387, 11–20 (2015).CAS 
PubMed 

Google Scholar 
Webb, C. T., Heinz, E. & Lithgow, T. Evolution of the β-barrel assembly machinery. Trends Microbiol. 20, 612–620 (2012).Article 
CAS 
PubMed 

Google Scholar 
Dunn, J. P., Kenedy, M. R., Iqbal, H. & Akins, D. R. Characterization of the β-barrel assembly machine accessory lipoproteins from Borrelia burgdorferi. BMC Microbiol. 15, 70 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Wu, T. et al. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121, 235–245 (2005).Article 
CAS 
PubMed 

Google Scholar 
O’Neil, P. K., Rollauer, S. E., Noinaj, N. & Buchanan, S. K. Fitting the pieces of the β-barrel assembly machinery complex. Biochemistry 54, 6303–6311 (2015).Article 
CAS 
PubMed 

Google Scholar 
Hart, E. M. & Silhavy, T. J. Functions of the BamBCDE lipoproteins revealed by bypass mutations in BamA. J. Bacteriol. 202, 10 (2020).Article 

Google Scholar 
Malinverni, J. C. et al. YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol. Microbiol. 61, 151–164 (2006).Article 
CAS 
PubMed 

Google Scholar 
Roman-Hernandez, G., Peterson, J. H. & Bernstein, H. D. Reconstitution of bacterial autotransporter assembly using purified components. Elife 3, e04234 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Hagan, C. L., Kim, S. & Kahne, D. Reconstitution of outer membrane protein assembly from purified components. Science 328, 890–892 (2010).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Jansen, K. B., Baker, S. L. & Sousa, M. C. Crystal structure of BamB bound to a periplasmic domain fragment of BamA, the central component of the β-barrel assembly machine. J. Biol. Chem. 290, 2126–2136 (2015).Article 
CAS 
PubMed 

Google Scholar 
Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Bergal, H. T., Hopkins, A. H., Metzner, S. I. & Sousa, M. C. The structure of a BamA-BamD fusion illuminates the architecture of the β-barrel assembly machine core. Structure 24, 243–251 (2016).Article 
CAS 
PubMed 

Google Scholar 
Chamachi, N. et al. Chaperones Skp and SurA dynamically expand unfolded OmpX and synergistically disassemble oligomeric aggregates. Proc. Natl. Acad. Sci. U S A 119, e2118919119 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Giuseppe, P. O., Von Atzingen, M., Nascimento, A. L., Zanchin, N. I. & Guimaraes, B. G. The crystal structure of the leptospiral hypothetical protein LIC12922 reveals homology with the periplasmic chaperone SurA. J. Struct. Biol. 173, 312–322 (2011).Article 
CAS 
PubMed 

Google Scholar 
Schiffrin, B. et al. Dynamic interplay between the periplasmic chaperone SurA and the BAM complex in outer membrane protein folding. Commun. Biol. 5, 560 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Vincent, A. T. et al. Revisiting the taxonomy and evolution of pathogenicity of the genus Leptospira through the prism of genomics. PLoS Negl. Trop. Dis. 13, e0007270 (2019).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Finn, R. D., Clements, J. & Eddy, S. R. HMMER web server: Interactive sequence similarity searching. Nucleic Acids Res. 39, W29-37 (2011).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Potter, S. C. et al. HMMER web server: 2018 update. Nucleic Acids Res. 46, W200–W204 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Reichenbach, H. The order cytophagales. In The prokaryotes (eds Dworkin, M. et al.) (Springer, 2006).
Google Scholar 
Dahal, R. H., Chaudhary, D. K., Kim, D. U. & Kim, J. Nine novel psychrotolerant species of the genus Pedobacter isolated from Arctic soil with potential antioxidant activities. Int. J. Syst. Evol. Microbiol. 70, 2537–2553 (2020).Article 
CAS 
PubMed 

Google Scholar 
Shi, W., Takano, T. & Liu, S. Anditalea andensis gen. nov., sp. nov., an alkaliphilic, halotolerant bacterium isolated from extreme alkali-saline soil. Antonie Van Leeuwenhoek 102, 703–710 (2012).Article 
CAS 
PubMed 

Google Scholar 
Zhang, L., Zhou, X. Y., Su, X. J., Hu, Q. & Jiang, J. D. Spirosoma sordidisoli sp. nov., a propanil-degrading bacterium isolated from a herbicide-contaminated soil. Antonie Van Leeuwenhoek 112, 1523–1532 (2019).Article 
CAS 
PubMed 

Google Scholar 
Anil Kumar, P. et al. Cecembia lonarensis gen. nov., sp. nov., a haloalkalitolerant bacterium of the family Cyclobacteriaceae, isolated from a haloalkaline lake and emended descriptions of the genera Indibacter, Nitritalea and Belliella. Int. J. Syst. Evol. Microbiol. 62, 2252–2258 (2012).Article 
CAS 
PubMed 

Google Scholar 
Jangir, P. K., Singh, A., Shivaji, S. & Sharma, R. Genome sequence of the alkaliphilic bacterium Nitritalea halalkaliphila type strain LW7, isolated from Lonar Lake, India. J. Bacteriol. 194, 5688–5689 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Anil Kumar, P., Srinivas, T. N., Madhu, S., Manorama, R. & Shivaji, S. Indibacter alkaliphilus gen. nov., sp. nov., an alkaliphilic bacterium isolated from a haloalkaline lake. Int. J. Syst. Evol. Microbiol. 60, 721–726 (2010).Article 
CAS 
PubMed 

Google Scholar 
Lim, S. B. Y. et al. Genome sequence of the tropical atmosphere bacterium Pontibacter sp. strain SGAir0037. Microbiol. Resour. Announc. 8, 10 (2019).Article 

Google Scholar 
Van Trappen, S., Vandecandelaere, I., Mergaert, J. & Swings, J. Flavobacterium degerlachei sp. nov., Flavobacterium frigoris sp. nov. and Flavobacterium micromati sp. nov., novel psychrophilic bacteria isolated from microbial mats in Antarctic lakes. Int. J. Syst. Evol. Microbiol. 54, 85–92 (2004).Article 
PubMed 

Google Scholar 
Onufryk, C., Crouch, M. L., Fang, F. C. & Gross, C. A. Characterization of six lipoproteins in the sigmaE regulon. J. Bacteriol. 187, 4552–4561 (2005).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Tellez, R. Jr. & Misra, R. Substitutions in the BamA β-barrel domain overcome the conditional lethal phenotype of a ΔbamB ΔbamE strain of Escherichia coli. J. Bacteriol. 194, 317–324 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wu, R., Stephenson, R., Gichaba, A. & Noinaj, N. The big BAM theory: An open and closed case?. Biochim. Biophys. Acta Biomembr. 1862, 183062 (2020).Article 
CAS 
PubMed 

Google Scholar 
Lenhart, T. R., Kenedy, M. R., Yang, X., Pal, U. & Akins, D. R. BB0324 and BB0028 are constituents of the Borrelia burgdorferi beta-barrel assembly machine (BAM) complex. BMC Microbiol. 12, 60 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Plummer, A. M. & Fleming, K. G. Bama alone accelerates outer membrane protein folding in vitro through a catalytic mechanism. Biochemistry 54, 6009–6011 (2015).Article 
CAS 
PubMed 

Google Scholar 
Estrada Mallarino, L. et al. TtOmp85, a β-barrel assembly protein, functions by barrel augmentation. Biochemistry 54, 844–852 (2015).Article 
CAS 
PubMed 

Google Scholar 
Sklar, J. G., Wu, T., Kahne, D. & Silhavy, T. J. Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev. 21, 2473–2484 (2007).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Alvira, S. et al. Inter-membrane association of the Sec and BAM translocons for bacterial outer-membrane biogenesis. Elife 9, e60669 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Marx, D. C. et al. SurA is a cryptically grooved chaperone that expands unfolded outer membrane proteins. Proc. Natl. Acad. Sci. U S A 117, 28026–28035 (2020).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Stroud, D. A. et al. Biogenesis of mitochondrial β-barrel proteins: the POTRA domain is involved in precursor release from the SAM complex. Mol. Biol. Cell 22, 2823–2833 (2011).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Dautin, N. Folding control in the path of type 5 secretion. Toxins (Basel) 13, 341 (2021).Article 
CAS 
PubMed 

Google Scholar 
Meuskens, I., Saragliadis, A., Leo, J. C. & Linke, D. Type V secretion systems: An overview of passenger domain functions. Front. Microbiol. 10, 1–19 (2019).Article 

Google Scholar 
Chatterjee, S., Basak, A. J., Nair, A. V., Duraivelan, K. & Samanta, D. Immunoglobulin-fold containing bacterial adhesins: Molecular and structural perspectives in host tissue colonization and infection. FEMS Microbiol. Lett. 368, fnaa220 (2021).Article 
CAS 
PubMed 

Google Scholar 
Nobbs, A. H., Shearer, B. H., Drobni, M., Jepson, M. A. & Jenkinson, H. F. Adherence and internalization of Streptococcus gordonii by epithelial cells involves beta1 integrin recognition by SspA and SspB (antigen I/II family) polypeptides. Cell Microbiol. 9, 65–83 (2007).Article 
CAS 
PubMed 

Google Scholar 
Jarva, M. A., Hirt, H., Dunny, G. M. & Berntsson, R. P. Polymer adhesindomains in Gram-positive cell surface proteins. Front. Microbiol. 11, 599899 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Monzon, V. & Bateman, A. Large-scale discovery of microbial fibrillar adhesins and identification of novel members of adhesive domain families. J. Bacteriol. 204, e0010722 (2022).Article 
PubMed 

Google Scholar 
Niemann, H. H., Schubert, W. D. & Heinz, D. W. Adhesins and invasins of pathogenic bacteria: A structural view. Microbes Infect. 6, 101–112 (2004).Article 
CAS 
PubMed 

Google Scholar 
Haake, D. A. & Matsunaga, J. Leptospiral immunoglobulin-like domain proteins: Roles in virulence and immunity. Front. Immunol. 11, 579907 (2020).Article 
CAS 
PubMed 

Google Scholar 
Hsieh, C. L. et al. Leptospira immunoglobulin-like protein B interacts with the 20th exon of human tropoelastin contributing to leptospiral adhesion to human lung cells. Front. Cell Infect. Microbiol. 7, 163 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
McBride, A. J. et al. Genetic diversity of the leptospiral immunoglobulin-like (Lig) genes in pathogenic Leptospira spp. Infect. Genet. Evol. 9, 196–205 (2009).Article 
CAS 
PubMed 

Google Scholar 
Matsunaga, J. et al. Pathogenic Leptospira species express surface-exposed proteins belonging to the bacterial immunoglobulin superfamily. Mol. Microbiol. 49, 929–945 (2003).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Domingos, R. F. et al. Features of two proteins of Leptospira interrogans with potential role in host-pathogen interactions. BMC Microbiol. 12, 50 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Hooda, Y. et al. Slam is an outer membrane protein that is required for the surface display of lipidated virulence factors in Neisseria. Nat. Microbiol. 1, 16009 (2016).Article 
CAS 
PubMed 

Google Scholar 
He, H. et al. A Borrelia burgdorferi LptD homolog is required for flipping of surface lipoproteins through the spirochetal outer membrane. Mol. Microbiol. 119, 752–767 (2023).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Ipe, D. S., Horton, E. & Ulett, G. C. The basics of bacteriuria: Strategies of microbes for persistence in urine. Front. Cell Infect. Microbiol. 6, 14 (2016).Article 
PubMed 
PubMed Central 

Google Scholar 
Bouatra, S. et al. The human urine metabolome. PLoS One 8, e73076 (2013).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Trueba, G., Zapata, S., Madrid, K., Cullen, P. & Haake, D. Cell aggregation: A mechanism of pathogenic Leptospira to survive in fresh water. Int. Microbiol. 7, 35–40 (2004).PubMed 

Google Scholar 
Casanovas-Massana, A. et al. Quantification of Leptospira interrogans survival in soil and water microcosms. Appl. Environ. Microbiol. 84, e00507 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Noguchi, H. The survival of Leptospira (Spirochaeta) Icterohaemorrhagiae in nature; observations concerning microchemical reactions and intermediary hosts. J. Exp. Med. 27, 609–625 (1918).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Nau, L. H., Obiegala, A., Krol, N., Mayer-Scholl, A. & Pfeffer, M. Survival time of Leptospira kirschneri serovar Grippotyphosa under different environmental conditions. PLoS One 15, e0236007 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Thiel, V. et al. Draft genome sequence of the moderately thermophilic bacterium Schleiferia thermophila strain yellowstone (Bacteroidetes). Genome Announc. 2, 10 (2014).Article 

Google Scholar 
Council, N. R. Guide for the care and use of laboratory animals 8th edn. (The National Academies Press, 2011).
Google Scholar 
Paysan-Lafosse, T. et al. InterPro in 2022. Nucleic Acids Res. 51, D418–D427 (2023).Article 
CAS 
PubMed 

Google Scholar 
Bendtsen, J. D., Nielsen, H., von Heijne, G. & Brunak, S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783–795 (2004).Article 
PubMed 

Google Scholar 
Pettersen, E. F. et al. UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).Article 
CAS 
PubMed 

Google Scholar 
da Cunha, C. E. P. et al. Evaluation of different strategies to promote a protective immune response against leptospirosis using a recombinant LigA and LigB chimera. Vaccine 37, 1844–1852 (2019).Article 
PubMed 

Google Scholar 
Jones, P. et al. InterProScan 5: Genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).Article 
PubMed 
PubMed Central 

Google Scholar 
Edgar, R. C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Gouy, M., Tannier, E., Comte, N. & Parsons, D. P. Seaview version 5: A multiplatform software for multiple sequence alignment, molecular phylogenetic analyses, and tree reconciliation. Methods Mol. Biol. 2231, 241–260 (2021).Article 
CAS 
PubMed 

Google Scholar 
Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000).Article 
CAS 
PubMed 

Google Scholar 
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Minh, B. Q. et al. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Ronquist, F. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).Article 
PubMed 
PubMed Central 

Google Scholar 

Hot Topics

Related Articles