Leptospira interrogans biofilm transcriptome highlights adaption to starvation and general stress while maintaining virulence.
Journal
NPJ biofilms and microbiomes
ISSN: 2055-5008
Titre abrégé: NPJ Biofilms Microbiomes
Pays: United States
ID NLM: 101666944
Informations de publication
Date de publication:
30 Sep 2024
30 Sep 2024
Historique:
received:
03
05
2024
accepted:
15
09
2024
medline:
1
10
2024
pubmed:
1
10
2024
entrez:
30
9
2024
Statut:
epublish
Résumé
Life-threatening Leptospira interrogans navigate a dual existence: surviving in the environment and infecting mammalian hosts. Biofilm formation is presumably an important survival strategy to achieve this process. Understanding the relation between biofilm and virulence might improve our comprehension of leptospirosis epidemiology. Our study focused on elucidating Leptospira's adaptations and regulations involved in such complex microenvironments. To determine the transcriptional profile of Leptospira in biofilm, we compared the transcriptomes in late biofilms and in exponential planktonic cultures. While genes for motility, energy production, and metabolism were downregulated, those governing general stress response, defense against metal stress, and redox homeostasis showed a significant upsurge, hinting at a tailored defensive strategy against stress. Further, despite a reduced metabolic state, biofilm disruption swiftly restored metabolic activity. Crucially, bacteria in late biofilms or resulting from biofilm disruption retained virulence in an animal model. In summary, our study highlights Leptospira's adaptive equilibrium in biofilms: minimizing energy expenditure, potentially aiding in withstanding stresses while maintaining pathogenicity. These insights are important for explaining the survival strategies of Leptospira, revealing that a biofilm lifestyle may confer an advantage in maintaining virulence, an understanding essential for managing leptospirosis across both environmental and mammalian reservoirs.
Identifiants
pubmed: 39349472
doi: 10.1038/s41522-024-00570-0
pii: 10.1038/s41522-024-00570-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
95Informations de copyright
© 2024. The Author(s).
Références
Costa, F. et al. Global morbidity and mortality of leptospirosis: a systematic review. PLoS Negl. Trop. Dis. 9, e0003898 (2015).
doi: 10.1371/journal.pntd.0003898
pubmed: 26379143
pmcid: 4574773
Adler, B. & de la Pena Moctezuma, A. Leptospira and leptospirosis. Vet. Microbiol 140, 287–296 (2009).
doi: 10.1016/j.vetmic.2009.03.012
pubmed: 19345023
Bierque, E., Thibeaux, R., Girault, D., Soupé-Gilbert, M. E. & Goarant, C. A systematic review of Leptospira in water and soil environments. PLoS ONE 15, e0227055 (2020).
doi: 10.1371/journal.pone.0227055
pubmed: 31986154
pmcid: 6984726
Thibeaux, R. et al. Seeking the environmental source of Leptospirosis reveals durable bacterial viability in river soils. PLoS Negl. Trop. Dis. 11, e0005414 (2017).
doi: 10.1371/journal.pntd.0005414
pubmed: 28241042
pmcid: 5344526
Yanagihara, Y. et al. Leptospira is an environmental bacterium that grows in waterlogged soil. Microbiol. Spectr. 10, e02157–21 (2022).
doi: 10.1128/spectrum.02157-21
pubmed: 35289672
pmcid: 9045322
Chadsuthi, S., Chalvet-Monfray, K., Wiratsudakul, A. & Modchang, C. The effects of flooding and weather conditions on leptospirosis transmission in Thailand. Sci. Rep. 11, 1486 (2021).
doi: 10.1038/s41598-020-79546-x
pubmed: 33452273
pmcid: 7810882
Ristow, P. et al. Biofilm formation by saprophytic and pathogenic leptospires. Microbiology 154, 1309–1317 (2008).
doi: 10.1099/mic.0.2007/014746-0
pubmed: 18451039
Singh, R. et al. Microbial diversity of biofilms in dental unit water systems. Appl. Environ. Microbiol. 69, 3412–3420 (2003).
doi: 10.1128/AEM.69.6.3412-3420.2003
pubmed: 12788744
pmcid: 161485
Kumar, K. V., Lall, C., Raj, R. V., Vedhagiri, K. & Vijayachari, P. Coexistence and survival of pathogenic leptospires by formation of biofilm with Azospirillum. FEMS Microbiol. Ecol. 91, fiv051 (2015).
Thibeaux, R. et al. The zoonotic pathogen Leptospira interrogans mitigates environmental stress through cyclic-di-GMP-controlled biofilm production. NPJ Biofilms Microbiomes 6, 24 (2020).
doi: 10.1038/s41522-020-0134-1
pubmed: 32532998
pmcid: 7293261
Santos, A. A. N. et al. Leptospira interrogans biofilm formation in Rattus norvegicus (Norway rats) natural reservoirs. PLoS Negl. Trop. Dis. 15, e0009736 (2021).
doi: 10.1371/journal.pntd.0009736
pubmed: 34495971
pmcid: 8451993
Ackermann, K. et al. In vivo biofilm formation of pathogenic Leptospira spp. in the vitreous humor of horses with recurrent uveitis. Microorganisms 9, 1915.
Brihuega, B., Samartino, L., Auteri, C., Venzano, A. & Caimi, K. In vivo cell aggregations of a recent swine biofilm-forming isolate of Leptospira interrogans strain from Argentina. Rev. Argent. Microbiol. 44, 138–143 (2012).
pubmed: 23102459
Goodman, A. L. et al. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 7, 745–754 (2004).
doi: 10.1016/j.devcel.2004.08.020
pubmed: 15525535
Roux, A. & Ghigo, J.-M. Les biofilms bactériens. Bull. l’Académie v.étérinaire Fr. 159, 261–268 (2006).
doi: 10.4267/2042/47842
Morot, A. et al. Virulence of Vibrio harveyi ORM4 towards the European abalone Haliotis tuberculata involves both quorum sensing and a type III secretion system. Environ. Microbiol. 23, 5273–5288 (2021).
doi: 10.1111/1462-2920.15592
pubmed: 33989448
Gostic, K. M. et al. Mechanistic dose-response modelling of animal challenge data shows that intact skin is a crucial barrier to leptospiral infection. Philos. Trans. R. Soc. Lond. Ser. B: Biol. Sci. 374, 20190367 (2019).
doi: 10.1098/rstb.2019.0367
Sato, Y. et al. Environmental DNA metabarcoding to detect pathogenic Leptospira and associated organisms in leptospirosis-endemic areas of Japan. Sci. Rep. 9, 6575 (2019).
doi: 10.1038/s41598-019-42978-1
pubmed: 31024059
pmcid: 6484013
Davignon, G. et al. Leptospirosis: toward a better understanding of the environmental lifestyle of Leptospira. Front. Water 5, 1195094 (2023).
doi: 10.3389/frwa.2023.1195094
Vallenet, D. et al. MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res. 34, 53–65 (2006).
doi: 10.1093/nar/gkj406
pubmed: 16407324
pmcid: 1326237
Kanehisa, M., Furumichi, M., Sato, Y., Kawashima, M. & Ishiguro-Watanabe, M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res. 51, D587–D592 (2023).
doi: 10.1093/nar/gkac963
pubmed: 36300620
Zhukova, A. et al. Genome-wide transcriptional start site mapping and sRNA identification in the pathogen leptospira interrogans. Front. Cell Infect. Microbiol. 7, 10 (2017).
doi: 10.3389/fcimb.2017.00010
pubmed: 28154810
pmcid: 5243855
Fule, L. et al. Role of the major determinant of polar flagellation FlhG in the endoflagella-containing spirochete Leptospira. Mol. Microbiol. 116, 1392–1406 (2021).
doi: 10.1111/mmi.14831
pubmed: 34657338
Minamino, T., Kinoshita, M. & Namba, K. Fuel of the bacterial flagellar type III protein export apparatus. Methods Mol. Biol. 1593, 3–16 (2017).
doi: 10.1007/978-1-4939-6927-2_1
pubmed: 28389941
Salah Ud-Din, A. I. M. & Roujeinikova, A. Methyl-accepting chemotaxis proteins: a core sensing element in prokaryotes and archaea. Cell Mol. Life Sci. 74, 3293–3303 (2017).
doi: 10.1007/s00018-017-2514-0
pubmed: 28409190
pmcid: 11107704
Gumerov, V. M., Ortega, D. R., Adebali, O., Ulrich, L. E. & Zhulin, I. B. MiST 3.0: an updated microbial signal transduction database with an emphasis on chemosensory systems. Nucleic Acids Res. 48, D459–D464 (2020).
doi: 10.1093/nar/gkz988
pubmed: 31754718
Rothfield, L. I. & Justice, S. S. Bacterial cell division: the cycle of the ring. Cell 88, 581–584 (1997).
doi: 10.1016/S0092-8674(00)81899-1
pubmed: 9054497
Camberg, J. L., Hoskins, J. R. & Wickner, S. The interplay of ClpXP with the cell division machinery in Escherichia coli. J. Bacteriol. 193, 1911–1918 (2011).
doi: 10.1128/JB.01317-10
pubmed: 21317324
pmcid: 3133021
Deng, X. et al. The structure of bactofilin filaments reveals their mode of membrane binding and lack of polarity. Nat. Microbiol 4, 2357–2368 (2019).
doi: 10.1038/s41564-019-0544-0
pubmed: 31501539
pmcid: 6881188
Kühn, J. et al. Bactofilins, a ubiquitous class of cytoskeletal proteins mediating polar localization of a cell wall synthase in Caulobacter crescentus. EMBO J. 29, 327–339 (2010).
doi: 10.1038/emboj.2009.358
pubmed: 19959992
Jackson, K. M., Schwartz, C., Wachter, J., Rosa, P. A. & Stewart, P. E. A widely conserved bacterial cytoskeletal component influences unique helical shape and motility of the spirochete Leptospira biflexa. Mol. Microbiol 108, 77–89 (2018).
doi: 10.1111/mmi.13917
pubmed: 29363884
pmcid: 5867249
Mishra, S., Misra, H. S. & Kota, S. FtsK, a DNA motor protein, coordinates the genome segregation and early cell division processes in Deinococcus radiodurans. mBio 13, e0174222 (2022).
doi: 10.1128/mbio.01742-22
pubmed: 36300930
Kobayashi, G., Moriya, S. & Wada, C. Deficiency of essential GTP-binding protein ObgE in Escherichia coli inhibits chromosome partition. Mol. Microbiol. 41, 1037–1051 (2001).
doi: 10.1046/j.1365-2958.2001.02574.x
pubmed: 11555285
Jorgenson, M. A., Chen, Y., Yahashiri, A., Popham, D. L. & Weiss, D. S. The bacterial septal ring protein RlpA is a lytic transglycosylase that contributes to rod shape and daughter cell separation in Pseudomonas aeruginosa. Mol. Microbiol. 93, 113–128 (2014).
doi: 10.1111/mmi.12643
pubmed: 24806796
pmcid: 4086221
Henneberry, R. C. & Cox, C. D. Beta-oxidation of fatty acids by Leptospira. Can. J. Microbiol. 16, 41–45 (1970).
doi: 10.1139/m70-007
pubmed: 5415967
Sørensen, M. A., Fricke, J. & Pedersen, S. Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo. J. Mol. Biol. 280, 561–569 (1998).
doi: 10.1006/jmbi.1998.1909
pubmed: 9677288
Starosta, A. L., Lassak, J., Jung, K. & Wilson, D. N. The bacterial translation stress response. FEMS Microbiol. Rev. 38, 1172–1201 (2014).
doi: 10.1111/1574-6976.12083
pubmed: 25135187
Del Peso Santos, T. et al. BipA exerts temperature-dependent translational control of biofilm-associated colony morphology in Vibrio cholerae. Elife. 10, e60607 (2021).
Choudhury, P. & Flower, A. M. Efficient assembly of ribosomes is inhibited by deletion of bipA in Escherichia coli. J. Bacteriol. 197, 1819–1827 (2015).
doi: 10.1128/JB.00023-15
pubmed: 25777676
pmcid: 4402399
Michaux, C. et al. CspR, a cold shock RNA-binding protein involved in the long-term survival and the virulence of Enterococcus faecalis. J. Bacteriol. 194, 6900–6908 (2012).
doi: 10.1128/JB.01673-12
pubmed: 23086208
pmcid: 3510560
Neidig, A. et al. TypA is involved in virulence, antimicrobial resistance and biofilm formation in Pseudomonas aeruginosa. BMC Microbiol. 13, 77 (2013).
doi: 10.1186/1471-2180-13-77
pubmed: 23570569
pmcid: 3639842
Hengge, R. Principles of c-di-GMP signalling in bacteria. Nat. Rev. 7, 263–273 (2009).
Xiao, G. et al. Identification and characterization of c-di-GMP metabolic enzymes of Leptospira interrogans and c-di-GMP fluctuations after thermal shift and infection. Front. Microbiol. 9, 764 (2018).
doi: 10.3389/fmicb.2018.00764
pubmed: 29755425
pmcid: 5932348
Vasconcelos, L. et al. Genomic insights into the c-di-GMP signaling and biofilm development in the saprophytic spirochete Leptospira biflexa. Arch. Microbiol. 205, 180 (2023).
doi: 10.1007/s00203-023-03519-7
pubmed: 37031284
Braun, V., Mahren, S. & Ogierman, M. Regulation of the FecI-type ECF sigma factor by transmembrane signalling. Curr. Opin. Microbiol. 6, 173–180 (2003).
doi: 10.1016/S1369-5274(03)00022-5
pubmed: 12732308
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).
doi: 10.1371/journal.ppat.1008904
pubmed: 33021995
pmcid: 7567364
Smaldone, G. T. & Helmann, J. D. CsoR regulates the copper efflux operon copZA in Bacillus subtilis. Microbiology (Reading) 153, 4123–4128 (2007).
doi: 10.1099/mic.0.2007/011742-0
pubmed: 18048925
Corbett, D. et al. The combined actions of the copper-responsive repressor CsoR and copper-metallochaperone CopZ modulate CopA-mediated copper efflux in the intracellular pathogen Listeria monocytogenes. Mol. Microbiol. 81, 457–472 (2011).
doi: 10.1111/j.1365-2958.2011.07705.x
pubmed: 21564342
Rademacher, C. & Masepohl, B. Copper-responsive gene regulation in bacteria. Microbiology (Reading) 158, 2451–2464 (2012).
doi: 10.1099/mic.0.058487-0
pubmed: 22918892
Chaplin, A. K., Tan, B. G., Vijgenboom, E. & Worrall, J. A. Copper trafficking in the CsoR regulon of Streptomyces lividans. Metallomics 7, 145–155 (2015).
doi: 10.1039/C4MT00250D
pubmed: 25409712
Andrei, A. et al. Cu homeostasis in bacteria: the Ins and Outs. Membranes 10, 242 (2020).
Nikaido, H. & Pagès, J. M. Broad-specificity efflux pumps and their role in multidrug resistance of Gram-negative bacteria. FEMS Microbiol. Rev. 36, 340–363 (2012).
doi: 10.1111/j.1574-6976.2011.00290.x
pubmed: 21707670
Subhadra, B. et al. Local repressor AcrR regulates AcrAB efflux pump required for biofilm formation and virulence in Acinetobacter nosocomialis. Front. Cell Infect. Microbiol. 8, 270 (2018).
doi: 10.3389/fcimb.2018.00270
pubmed: 30131944
pmcid: 6090078
Busenlehner, L. S., Pennella, M. A. & Giedroc, D. P. The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance. FEMS Microbiol. Rev. 27, 131–143 (2003).
doi: 10.1016/S0168-6445(03)00054-8
pubmed: 12829264
Liu, T. et al. A novel cyanobacterial SmtB/ArsR family repressor regulates the expression of a CPx-ATPase and a metallothionein in response to both Cu(I)/Ag(I) and Zn(II)/Cd(II). J. Biol. Chem. 279, 17810–17818 (2004).
doi: 10.1074/jbc.M310560200
pubmed: 14960585
Zhi, F. et al. An ArsR transcriptional regulator facilitates Brucella sp. survival via regulating self and outer membrane protein. Int. J. Mol. Sci. 22, 10860 (2021).
Giraud-Gatineau, A. et al. Evolutionary insights into the emergence of virulent Leptospira spirochetes. PLoS Pathog 20, e1012161 (2021).
doi: 10.1371/journal.ppat.1012161
Yin, W., Wang, Y., Liu, L. & He, J. Biofilms: the microbial “protective clothing” in extreme environments. Int. J. Mol. Sci. 20, 3423 (2019).
Sharma, S. et al. Microbial biofilm: a review on formation, infection, antibiotic resistance, control measures, and innovative treatment. Microorganisms 11, 1614 (2023).
doi: 10.3390/microorganisms11061614
pubmed: 37375116
pmcid: 10305407
Iraola, G. et al. Transcriptome sequencing reveals wide expression reprogramming of basal and unknown genes in Leptospira biflexa biofilms. mSphere 1, e00042–16 (2016).
doi: 10.1128/mSphere.00042-16
pubmed: 27303713
pmcid: 4863578
Lin, T., Gao, L., Zhao, X., Liu, J. & Norris, S. J. Mutations in the Borrelia burgdorferi flagellar type III secretion system genes fliH and fliI profoundly affect spirochete flagellar assembly, morphology, motility, structure, and cell division. mBio 6, e00579–15 (2015).
doi: 10.1128/mBio.00579-15
pubmed: 25968649
pmcid: 4436065
Wunder, E. A. et al. A novel flagellar sheath protein, FcpA, determines filament coiling, translational motility and virulence for the Leptospira spirochete. Mol. Microbiol. 101, 457–470 (2016).
doi: 10.1111/mmi.13403
pubmed: 27113476
pmcid: 4979076
Wunder, E. A. Jr et al. FcpB is a surface filament protein of the endoflagellum required for the motility of the Spirochete Leptospira. Front. Cell Infect. Microbiol. 8, 130 (2018).
doi: 10.3389/fcimb.2018.00130
pubmed: 29868490
pmcid: 5953323
Lambert, A. et al. FlaA proteins in Leptospira interrogans are essential for motility and virulence, but not required for the formation of flagella sheath. Infect. Immun. 80, 2019–2025 (2012).
doi: 10.1128/IAI.00131-12
pubmed: 22451522
pmcid: 3370569
Gibson, K. H. et al. An asymmetric sheath controls flagellar supercoiling and motility in the leptospira spirochete. eLife 9, e53672 (2020).
doi: 10.7554/eLife.53672
pubmed: 32157997
pmcid: 7065911
Mercer, K. L. & Weiss, D. S. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J. Bacteriol. 184, 904–912 (2002).
doi: 10.1128/jb.184.4.904-912.2002
pubmed: 11807049
pmcid: 134820
Marmont, L. S. & Bernhardt, T. G. A conserved subcomplex within the bacterial cytokinetic ring activates cell wall synthesis by the FtsW-FtsI synthase. Proc. Natl Acad. Sci. USA 117, 23879–23885 (2020).
doi: 10.1073/pnas.2004598117
pubmed: 32907942
pmcid: 7519343
Slamti, L., de Pedro, M. A., Guichet, E. & Picardeau, M. Deciphering morphological determinants of the helix-shaped Leptospira. J. Bacteriol. 193, 6266–6275 (2011).
doi: 10.1128/JB.05695-11
pubmed: 21926230
pmcid: 3209227
Allaman, I., Bélanger, M. & Magistretti, P. J. Methylglyoxal, the dark side of glycolysis. Front. Neurosci. 9, 23 (2015).
doi: 10.3389/fnins.2015.00023
pubmed: 25709564
pmcid: 4321437
Cooper, R. A. Metabolism of methylglyoxal in microorganisms. Annu. Rev. Microbiol. 38, 49–68 (1984).
doi: 10.1146/annurev.mi.38.100184.000405
pubmed: 6093685
MacLean, M. J., Ness, L. S., Ferguson, G. P. & Booth, I. R. The role of glyoxalase I in the detoxification of methylglyoxal and in the activation of the KefB K+ efflux system in Escherichia coli. Mol. Microbiol. 27, 563–571 (1998).
doi: 10.1046/j.1365-2958.1998.00701.x
pubmed: 9489668
Kim, J. C., Oh, E., Kim, J. & Jeon, B. Regulation of oxidative stress resistance in Campylobacter jejuni, a microaerophilic foodborne pathogen. Front. Microbiol. 6, 751 (2015).
doi: 10.3389/fmicb.2015.00751
pubmed: 26284041
pmcid: 4518328
Resch, A., Rosenstein, R., Nerz, C. & Götz, F. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl. Environ. Microbiol. 71, 2663–2676 (2005).
doi: 10.1128/AEM.71.5.2663-2676.2005
pubmed: 15870358
pmcid: 1087559
Kalmokoff, M. et al. Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J. Bacteriol. 188, 4312–4320 (2006).
doi: 10.1128/JB.01975-05
pubmed: 16740937
pmcid: 1482957
Ram, R. J. et al. Community proteomics of a natural microbial biofilm. Science 308, 1915–1920 (2005).
Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W. & Davies, D. G. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184, 1140–1154 (2002).
doi: 10.1128/jb.184.4.1140-1154.2002
pubmed: 11807075
pmcid: 134825
van Vliet, A. H., Ketley, J. M., Park, S. F. & Penn, C. W. The role of iron in Campylobacter gene regulation, metabolism and oxidative stress defense. FEMS Microbiol. Rev. 26, 173–186 (2002).
doi: 10.1111/j.1574-6976.2002.tb00609.x
pubmed: 12069882
Kim, Y. H. et al. The role of periplasmic antioxidant enzymes (superoxide dismutase and thiol peroxidase) of the Shiga toxin-producing Escherichia coli O157:H7 in the formation of biofilms. Proteomics 6, 6181–6193 (2006).
doi: 10.1002/pmic.200600320
pubmed: 17133368
Fuzi, M. & Csoka, R. Differentiation of pathogenic and saprophytic Leptospira with a copper sulfate test. Zentralbl Bakteriol. 179, 231–237 (1960).
pubmed: 13849882
Falcone, E. et al. Revisiting the pro-oxidant activity of copper: interplay of ascorbate, cysteine, and glutathione. Metallomics 15, (2023).
Macomber, L. & Imlay, J. A. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl Acad. Sci. USA 106, 8344–8349 (2009).
doi: 10.1073/pnas.0812808106
pubmed: 19416816
pmcid: 2688863
Alav, I., Sutton, J. M. & Rahman, K. M. Role of bacterial efflux pumps in biofilm formation. J. Antimicrobial Chemother. 73, 2003–2020 (2018).
doi: 10.1093/jac/dky042
Baker, J. et al. Copper stress induces a global stress response in Staphylococcus aureus and represses sae and agr expression and biofilm formation. Appl. Environ. Microbiol. 76, 150–160 (2010).
doi: 10.1128/AEM.02268-09
pubmed: 19880638
Singh, K., Senadheera, D. B., Lévesque, C. M. & Cvitkovitch, D. G. The copYAZ operon functions in copper efflux, biofilm formation, genetic transformation, and stress tolerance in Streptococcus mutans. J. Bacteriol. 197, 2545–2557 (2015).
doi: 10.1128/JB.02433-14
pubmed: 26013484
pmcid: 4518833
Cusick, K. D., Dale, J. R., Fitzgerald, L. A., Little, B. J. & Biffinger, J. C. Adaptation to copper stress influences biofilm formation in Alteromonas macleodii. Biofouling 33, 505–519 (2017).
doi: 10.1080/08927014.2017.1329423
pubmed: 28604167
Williams, C. L. et al. Copper resistance of the emerging pathogen Acinetobacter baumannii. Appl Environ. Microbiol 82, 6174–6188 (2016).
doi: 10.1128/AEM.01813-16
pubmed: 27520808
pmcid: 5068154
Mouville, C. & Benaroudj, N. Survival tests for Leptospira spp. Methods Mol. Biol. 2134, 215–228 (2020).
Thibeaux, R. et al. Rainfall-driven resuspension of pathogenic Leptospira in a leptospirosis hotspot. Sci. total Environ. 911, 168700 (2024).
doi: 10.1016/j.scitotenv.2023.168700
pubmed: 37992819
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
doi: 10.1038/nmeth.2019
pubmed: 22743772
Zavala-Alvarado, C. & Benaroudj, N. The single-step method of RNA purification applied to Leptospira. Methods Mol. Biol. 2134, 41–51 (2020).
Cokelaer, T., Desvillechabrol, D., Legendre, R. & Cardon, M. Sequana’: a Set of Snakemake NGS pipelines. J. Open Source Softw. 2, 352 (2017).
doi: 10.21105/joss.00352
Köster, J. & Rahmann, S. Snakemake–a scalable bioinformatics workflow engine. Bioinformatics 28, 2520–2522 (2012).
doi: 10.1093/bioinformatics/bts480
pubmed: 22908215
Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).
doi: 10.1093/bioinformatics/bty560
pubmed: 30423086
pmcid: 6129281
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
doi: 10.1038/nmeth.1923
pubmed: 22388286
pmcid: 3322381
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
doi: 10.1093/bioinformatics/btt656
pubmed: 24227677
Ewels, P., Magnusson, M., Lundin, S. & Käller, M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32, 3047–3048 (2016).
doi: 10.1093/bioinformatics/btw354
pubmed: 27312411
pmcid: 5039924
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
doi: 10.1186/s13059-014-0550-8
pubmed: 25516281
pmcid: 4302049
Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).
doi: 10.1093/nar/gkv007
pubmed: 25605792
pmcid: 4402510
Merien, F., Amouriaux, P., Perolat, P., Baranton, G. & Saint Girons, I. Polymerase chain reaction for detection of Leptospira spp. in clinical samples. J. Clin. Microbiol 30, 2219–2224 (1992).
doi: 10.1128/jcm.30.9.2219-2224.1992
pubmed: 1400983
pmcid: 265482
Straume, D., Piechowiak, K. W., Kjos, M. & Håvarstein, L. S. Class A PBPs: It is time to rethink traditional paradigms. Mol. Microbiol 116, 41–52 (2021).
doi: 10.1111/mmi.14714
pubmed: 33709487
Miyachiro, M. M., Contreras-Martel, C. & Dessen, A. Penicillin-binding proteins (PBPs) and bacterial cell wall elongation complexes. Subcell. Biochem 93, 273–289 (2019).
doi: 10.1007/978-3-030-28151-9_8
pubmed: 31939154
Szwedziak, P. & Löwe, J. Do the divisome and elongasome share a common evolutionary past? Curr. Opin. Microbiol 16, 745–751 (2013).
doi: 10.1016/j.mib.2013.09.003
pubmed: 24094808