in

Resolving the conflict between antibiotic production and rapid growth by recognition of peptidoglycan of susceptible competitors

  • 1.

    Flemming, H. C. & Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat. Rev. Microbiol. 17, 247–260 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • 2.

    Hou, Q. & Kolodkin-Gal, I. Harvesting the complex pathways of antibiotic production and resistance of soil bacilli for optimizing plant microbiome. FEMS Microbiol Ecol., https://doi.org/10.1093/femsec/fiaa142 (2020).

  • 3.

    Frost, I. et al. Cooperation, competition and antibiotic resistance in bacterial colonies. ISME J. 12, 1582–1593 (2018).

    MathSciNet 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 4.

    Niehus, R. & Mitri, S. Handling unpredictable ecosystems. Nat. Ecol. Evol. 2, 1207–1208 (2018).

    PubMed 

    Google Scholar 

  • 5.

    Cordero, O. X. et al. Ecological populations of bacteria act as socially cohesive units of antibiotic production and resistance. Science 337, 1228–1231 (2012).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 6.

    Zhu, H., Sandiford, S. K. & van Wezel, G. P. Triggers and cues that activate antibiotic production by actinomycetes. J. Ind. Microbiol Biotechnol. 41, 371–386 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • 7.

    Arakawa, K. Manipulation of metabolic pathways controlled by signaling molecules, inducers of antibiotic production, for genome mining in Streptomyces spp. Antonie Van. Leeuwenhoek 111, 743–751 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • 8.

    Cornforth, D. M. & Foster, K. R. Competition sensing: the social side of bacterial stress responses. Nat. Rev. Microbiol 11, 285–293 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • 9.

    Westhoff, S., Kloosterman, A. M., van Hoesel, S. F. A., van Wezel, G. P. & Rozen, D. E. Competition sensing changes antibiotic production in streptomyces. mBio. 12, https://doi.org/10.1128/mBio.02729-20 (2021).

  • 10.

    Hou, Q. et al. Weaponizing volatiles to inhibit competitor biofilms from a distance. NPJ Biofilms Microbiomes 7, 2 (2021).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 11.

    Shank, E. A. Considering the lives of microbes in microbial communities. mSystems 3, https://doi.org/10.1128/mSystems.00155-17 (2018).

  • 12.

    Shank, E. A. et al. Interspecies interactions that result in Bacillus subtilis forming biofilms are mediated mainly by members of its own genus. Proc. Natl Acad. Sci. USA 108, E1236–E1243 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 13.

    Lyons, N. A., Kraigher, B., Stefanic, P., Mandic-Mulec, I. & Kolter, R. A combinatorial kin discrimination system in Bacillus subtilis. Curr. Biol. 26, 733–742 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 14.

    Stefanic, P., Kraigher, B., Lyons, N. A., Kolter, R. & Mandic-Mulec, I. Kin discrimination between sympatric Bacillus subtilis isolates. Proc. Natl Acad. Sci. USA 112, 14042–14047 (2015).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 15.

    Kalamara, M., Spacapan, M., Mandic-Mulec, I. & Stanley-Wall, N. R. Social behaviours by Bacillus subtilis: quorum sensing, kin discrimination and beyond. Mol. Microbiol. 110, 863–878 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 16.

    Harris, K. D. & Kolodkin-Gal, I. Applying the handicap principle to biofilms: condition-dependent signalling in Bacillus subtilis microbial communities. Environ. Microbiol., https://doi.org/10.1111/1462-2920.14497 (2018).

  • 17.

    Dorrestein, P. C. & Kelleher, N. L. Dissecting non-ribosomal and polyketide biosynthetic machineries using electrospray ionization Fourier-Transform mass spectrometry. Nat. Prod. Rep. 23, 893–918 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • 18.

    Bloudoff, K. & Schmeing, T. M. Structural and functional aspects of the nonribosomal peptide synthetase condensation domain superfamily: discovery, dissection and diversity. Biochim Biophys. Acta Proteins Proteom. 1865, 1587–1604 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • 19.

    Butcher, R. A. et al. The identification of bacillaene, the product of the PksX megacomplex in Bacillus subtilis. Proc. Natl Acad. Sci. USA 104, 1506–1509 (2007).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 20.

    Tsuge, K., Ano, T. & Shoda, M. Isolation of a gene essential for biosynthesis of the lipopeptide antibiotics plipastatin B1 and surfactin in Bacillus subtilis YB8. Arch. Microbiol. 165, 243–251 (1996).

    CAS 
    PubMed 

    Google Scholar 

  • 21.

    Coutte, F. et al. Effect of pps disruption and constitutive expression of srfA on surfactin productivity, spreading and antagonistic properties of Bacillus subtilis 168 derivatives. J. Appl Microbiol. 109, 480–491 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • 22.

    Hilton, M. D., Alaeddinoglu, N. G. & Demain, A. L. Synthesis of bacilysin by Bacillus subtilis branches from prephenate of the aromatic amino acid pathway. J. Bacteriol. 170, 482–484 (1988).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 23.

    Zheng, G., Hehn, R. & Zuber, P. Mutational analysis of the sbo-alb locus of Bacillus subtilis: identification of genes required for subtilosin production and immunity. J. Bacteriol. 182, 3266–3273 (2000).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 24.

    De Gonzalo, C. V. G., Zhu, L. Y., Oman, T. J. & van der Donk, W. A. NMR structure of the S-linked glycopeptide sublancin 168. Acs Chem. Biol. 9, 796–801 (2014).

    Google Scholar 

  • 25.

    Ongena, M. & Jacques, P. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16, 115–125 (2008).

    CAS 
    PubMed 

    Google Scholar 

  • 26.

    Magnuson, R., Solomon, J. & Grossman, A. D. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77, 207–216 (1994).

    CAS 
    PubMed 

    Google Scholar 

  • 27.

    Nakano, M. M. et al. Srfa is an operon required for surfactin production, competence development, and efficient sporulation in Bacillus-Subtilis. J. Bacteriol. 173, 1770–1778 (1991).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 28.

    Danevcic, T. et al. Surfactin facilitates horizontal gene transfer in Bacillus subtilis. Front. Microbiol. 12, doi:ARTN 657407 https://doi.org/10.3389/fmicb.2021.657407 (2021).

  • 29.

    Kluge, B., Vater, J., Salnikow, J. & Eckart, K. Studies on the biosynthesis of surfactin, a lipopeptide antibiotic from Bacillus-Subtilis Atcc-21332. Febs Lett. 231, 107–110 (1988).

    CAS 
    PubMed 

    Google Scholar 

  • 30.

    Gonzalez, D. J. et al. Microbial competition between Bacillus subtilis and Staphylococcus aureus monitored by imaging mass spectrometry. Microbiology 157, 2485–2492 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 31.

    Rosenberg, G. et al. Not so simple, not so subtle: the interspecies competition between Bacillus simplex and Bacillus subtilis and its impact on the evolution of biofilms. NPJ Biofilms Microbiomes 2, 15027 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 32.

    Falardeau, J., Wise, C., Novitsky, L. & Avis, T. J. Ecological and mechanistic insights into the direct and indirect antimicrobial properties of Bacillus subtilis lipopeptides on plant pathogens. J. Chem. Ecol. 39, 869–878 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • 33.

    Hoe, B. C., Gorzelnik, K. V., Yang, J. Y., Hendricks, N. & Dorrestein, P. C. Enzymatic resistance to the lipopeptide surfactin as identi fi ed through imaging mass spectrometry of bacterial competition. https://doi.org/10.1073/pnas.1205586109/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1205586109 (2012).

  • 34.

    Watrous, J. et al. Mass spectral molecular networking of living microbial colonies. Proc. Natl Acad. Sci. USA 109, E1743–E1752 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 35.

    Hu, F. X., Liu, Y. Y. & Li, S. Rational strain improvement for surfactin production: enhancing the yield and generating novel structures. Microbial Cell Factor. 18, https://doi.org/10.1186/s12934-019-1089-x (2019).

  • 36.

    Grau, A., Go, J. C. & Ortiz, A. A study on the interactions of surfactin with phospholipid vesicles. Biochim. Biophys. Acta. 1418, 307–319 (1999).

  • 37.

    Straight, P. D., Fischbach, M. A., Walsh, C. T., Rudner, D. Z. & Kolter, R. A singular enzymatic megacomplex from Bacillus subtilis. Proc. Natl Acad. Sci. USA 104, 305–310 (2007).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 38.

    Vargas-Bautista, C., Rahlwes, K. & Straight, P. Bacterial competition reveals differential regulation of the pks genes by Bacillus subtilis. J. Bacteriol. 196, 717–728 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 39.

    Rajavel, M., Mitra, A. & Gopal, B. Role of Bacillus subtilis BacB in the synthesis of bacilysin. J. Biol. Chem. 284, 31882–31892 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 40.

    Chen, X. H. et al. Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J. Biotechnol. 140, 38–44 (2009).

    CAS 
    PubMed 

    Google Scholar 

  • 41.

    Wu, L. M. et al. Difficidin and bacilysin from Bacillus amyloliquefaciens FZB42 have antibacterial activity against Xanthomonas oryzae rice pathogens. Sci. Rep. 5, https://doi.org/10.1038/srep12975 (2015).

  • 42.

    Inaoka, T., Takahashi, K., Ohnishi-Kameyama, M., Yoshida, M. & Ochi, K. Guanine nucleotides guanosine 5’-diphosphate 3’-diphosphate and GTP co-operatively regulate the production of an antibiotic bacilysin in Bacillus subtilis. J. Biol. Chem. 278, 2169–2176 (2003).

    CAS 
    PubMed 

    Google Scholar 

  • 43.

    Rapp, C., Jung, G., Katzer, W. & Loeffler, W. Chlorotetain from Bacillus-Subtilis, an antifungal dipeptide with an unusual chlorine-containing amino-acid. Angew. Chem. Int Ed. 27, 1733–1734 (1988).

    Google Scholar 

  • 44.

    Phister, T. G., O’Sullivan, D. J. & McKay, L. L. Identification of bacilysin, chlorotetaine, and iturin a produced by Bacillus sp. strain CS93 isolated from pozol, a Mexican fermented maize dough. Appl Environ. Microbiol 70, 631–634 (2004).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 45.

    Tsuge, K., Ano, T., Hirai, M., Nakamura, Y. & Shoda, M. The genes degQ, pps, and lpa-8 (sfp) are responsible for conversion of Bacillus subtilis 168 to plipastatin production. Antimicrob. Agents Chemother. 43, 2183–2192 (1999).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 46.

    Msadek, T., Kunst, F., Klier, A. & Rapoport, G. DegS-DegU and ComP-ComA modulator-effector pairs control expression of the Bacillus subtilis pleiotropic regulatory gene degQ. J. Bacteriol. 173, 2366–2377 (1991).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 47.

    Verhamme, D. T., Kiley, T. B. & Stanley-Wall, N. R. DegU co-ordinates multicellular behaviour exhibited by Bacillus subtilis. Mol. Microbiol. 65, 554–568 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • 48.

    Comella, N. & Grossman, A. D. Conservation of genes and processes controlled by the quorum response in bacteria: characterization of genes controlled by the quorum-sensing transcription factor ComA in Bacillus subtilis. Mol. Microbiol. 57, 1159–1174 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • 49.

    Wolf, D. et al. The quorum-sensing regulator ComA from Bacillus subtilis activates transcription using topologically distinct DNA motifs. Nucleic Acids Res. 44, 2160–2172 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • 50.

    Koroglu, T. E., Ogulur, I., Mutlu, S., Yazgan-Karatas, A. & Ozcengiz, G. Global regulatory systems operating in Bacilysin biosynthesis in Bacillus subtilis. J. Mol. Microbiol Biotechnol. 20, 144–155 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • 51.

    Ceyhan, D. I., Celekli, A. & Can, C. Relationship between soil composition, diversity and antifungal properties of Bacillus spp. isolated from southeastern Anatolia. Biotechnol. Biotec. Eq. 33, 170–177 (2019).

    CAS 

    Google Scholar 

  • 52.

    Saxena, A. K., Kumar, M., Chakdar, H., Anuroopa, N. & Bagyaraj, D. J. Bacillus species in soil as a natural resource for plant health and nutrition. J. Appl. Microbiol. 128, 1583–1594 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • 53.

    Arnaouteli, S., Bamford, N. C., Stanley-Wall, N. R. & Kovacs, A. T. Bacillus subtilis biofilm formation and social interactions. Nat. Rev. Microbiol., https://doi.org/10.1038/s41579-021-00540-9 (2021).

  • 54.

    Dergham, Y. et al. Comparison of the genetic features involved in Bacillus subtilis biofilm formation using multi-culturing approaches. Microorganisms 9, https://doi.org/10.3390/microorganisms9030633 (2021).

  • 55.

    Oppenheimer-Shaanan, Y. et al. Spatio-temporal assembly of functional mineral scaffolds within microbial biofilms. NPJ Biofilms Microbiomes 2, 15031 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 56.

    Barabesi, C. et al. Bacillus subtilis gene cluster involved in calcium carbonate biomineralization. J. Bacteriol. 189, 228–235 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • 57.

    Marvasi, M., Visscher, P. T., Perito, B., Mastromei, G. & Casillas-Martinez, L. Physiological requirements for carbonate precipitation during biofilm development of Bacillus subtilis etfA mutant. FEMS Microbiol Ecol. 71, 341–350 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • 58.

    Richter, M. & Rossello-Mora, R. Shifting the genomic gold standard for the prokaryotic species definition. P Natl Acad. Sci. USA 106, 19126–19131 (2009).

    ADS 
    CAS 

    Google Scholar 

  • 59.

    Goldoni, M. & Johansson, C. A mathematical approach to study combined effects of toxicants in vitro: Evaluation of the Bliss independence criterion and the Loewe additivity model. Toxicol. Vitr. 21, 759–769 (2007).

  • 60.

    Fan, F. & Wood, K. V. Bioluminescent assays for high-throughput screening. Assay. Drug Dev. Technol. 5, 127–136 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • 61.

    McLoon, A. L., Kolodkin-Gal, I., Rubinstein, S. M., Kolter, R. & Losick, R. Spatial regulation of histidine kinases governing biofilm formation in Bacillus subtilis. J. Bacteriol. 193, 679–685 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • 62.

    Irazoki, O., Hernandez, S. B. & Cava, F. Peptidoglycan muropeptides: release, perception, and functions as signaling molecules. Front. Microbiol. 10, https://doi.org/10.3389/fmicb.2019.00500 (2019).

  • 63.

    Virmani, R. et al. The Ser/Thr protein kinase PrkC imprints phenotypic memory in Bacillus anthracis spores by phosphorylating the glycolytic enzyme enolase. J. Biol. Chem. 294, 8930–8941 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 64.

    Lopez, D., Vlamakis, H. & Kolter, R. Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol Rev. 33, 152–163 (2009).

    CAS 
    PubMed 

    Google Scholar 

  • 65.

    Libby, E. A., Goss, L. A. & Dworkin, J. The eukaryotic-like Ser/Thr kinase PrkC regulates the essential WalRK two-component system in Bacillus subtilis. PLoS Genet. 11, e1005275 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 66.

    Rismondo, J., Percy, M. G. & Grundling, A. Discovery of genes required for lipoteichoic acid glycosylation predicts two distinct mechanisms for wall teichoic acid glycosylation. J. Biol. Chem. 293, 3293–3306 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 67.

    Audisio, M. C. Gram-positive bacteria with probiotic potential for the Apis mellifera L. Honey Bee: the experience in the Northwest of Argentina. Probiotics Antimicrob. Proteins 9, 22–31 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • 68.

    Emmert, E. A. & Handelsman, J. Biocontrol of plant disease: a (gram-) positive perspective. FEMS Microbiol. Lett. 171, 1–9 (1999).

    CAS 
    PubMed 

    Google Scholar 

  • 69.

    Bais, H. P., Fall, R. & Vivanco, J. M. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 134, 307–319 (2004).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 70.

    Raaijmakers, J. M., De Bruijn, I., Nybroe, O. & Ongena, M. Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol. Rev. 34, 1037–1062 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • 71.

    Gibbs, K. A., Urbanowski, M. L. & Greenberg, E. P. Genetic determinants of self identity and social recognition in bacteria. Science 321, 256–259 (2008).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 72.

    Wenren, L. M., Sullivan, N. L., Cardarelli, L., Septer, A. N. & Gibbs, K. A. Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. mBio. 4, https://doi.org/10.1128/mBio.00374-13 (2013).

  • 73.

    Hou, Q. & Kolodkin-Gal, I. Harvesting the complex pathways of antibiotic production and resistance of soil bacilli for optimizing plant microbiome. FEMS Microbiol. Ecol. 96, https://doi.org/10.1093/femsec/fiaa142 (2020).

  • 74.

    Shivers, R. P. & Sonenshein, A. L. Activation of the Bacillus subtilis global regulator CodY by direct interaction with branched-chain amino acids. Mol. Microbiol. 53, 599–611 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • 75.

    Zhang, Z. R. et al. Antibiotic production in Streptomyces is organized by a division of labor through terminal genomic differentiation. Sci. Adv. 6, https://doi.org/10.1126/sciadv.aay5781 (2020).

  • 76.

    Vollmer, W., Blanot, D. & de Pedro, M. A. Peptidoglycan structure and architecture. FEMS Microbiol Rev. 32, 149–167 (2008).

    CAS 
    PubMed 

    Google Scholar 

  • 77.

    Bhavsar, A. P. & Brown, E. D. Cell wall assembly in Bacillus subtilis: how spirals and spaces challenge paradigms. Mol. Microbiol. 60, 1077–1090 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • 78.

    Korgaonkar, A., Trivedi, U., Rumbaugh, K. P. & Whiteley, M. Community surveillance enhances Pseudomonas aeruginosa virulence during polymicrobial infection. Proc. Natl Acad. Sci. USA 110, 1059–1064 (2013).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 79.

    Korgaonkar, A. K. & Whiteley, M. Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan. J. Bacteriol. 193, 909–917 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • 80.

    Sicard, J. F. et al. N-Acetyl-glucosamine influences the biofilm formation of Escherichia coli. Gut Pathog. 10, 26 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 81.

    Aliashkevich, A., Alvarez, L. & Cava, F. New insights into the mechanisms and biological roles of D-amino acids in complex eco-systems. Front. Microbiol. 9, 683 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 82.

    Rigali, S. et al. Feast or famine: The global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep. 9, 670–675 (2008).

  • 83.

    Vollmer, W. Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev. 32, 287–306 (2008).

    CAS 
    PubMed 

    Google Scholar 

  • 84.

    Kim, S. J., Chang, J. & Singh, M. Peptidoglycan architecture of Gram-positive bacteria by solid-state NMR. Biochim Biophys. Acta 1848, 350–362 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • 85.

    Vetsigian, K., Jajoo, R. & Kishony, R. Structure and evolution of Streptomyces interaction networks in soil and in silico. PLoS Biol. 9, e1001184 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 86.

    Cuthbertson, L. & Nodwell, J. R. The TetR family of regulators. Microbiol Mol. Biol. Rev. 77, 440–475 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 87.

    Cava, F., de Pedro, M. A., Lam, H., Davis, B. M. & Waldor, M. K. Distinct pathways for modification of the bacterial cell wall by non-canonical D-amino acids. EMBO J. 30, 3442–3453 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 88.

    van der Es, D., Hogendorf, W. F., Overkleeft, H. S., van der Marel, G. A. & Codee, J. D. Teichoic acids: synthesis and applications. Chem. Soc. Rev. 46, 1464–1482 (2017).

    PubMed 

    Google Scholar 

  • 89.

    Egan, A. J. F., Errington, J. & Vollmer, W. Regulation of peptidoglycan synthesis and remodelling. Nat. Rev. Microbiol. 18, 446–460 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • 90.

    Dubnau, D. Genetic competence in Bacillus subtilis. Microbiol Rev. 55, 395–424 (1991).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 91.

    Stefanic, P. et al. Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis. Nat. Commun. 12, 3457 (2021).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 92.

    Salvadori, G., Junges, R., Morrison, D. A. & Petersen, F. C. Competence in Streptococcus pneumoniae and close commensal relatives: mechanisms and implications. Front. Cell Infect. Microbiol. 9, 94 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 93.

    Jowett, G. H. Statistical-methods for research workers – Fisher, Ra. R. Stat. Soc. C.-Appl. 5, 68–70 (1956).

    Google Scholar 

  • 94.

    Farzand, A. et al. Marker assisted detection and LC-MS analysis of antimicrobial compounds in different Bacillus strains and their antifungal effect on Sclerotinia sclerotiorum. Biol. Control 133, 91–102 (2019).

    CAS 

    Google Scholar 

  • 95.

    Paksanont, S. et al. Effect of temperature on Burkholderia pseudomallei growth, proteomic changes, motility and resistance to stress environments. Sci. Rep. 8, 9167 (2018).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 96.

    Andreevskaya, M. et al. Food spoilage-associated Leuconostoc, Lactococcus, and Lactobacillus species display different survival strategies in response to competition. Appl. Environ. Microbiol. 84, https://doi.org/10.1128/AEM.00554-18 (2018).

  • 97.

    Ju, S. Y. et al. Isolation and optimal fermentation condition of the Bacillus subtilis Subsp. natto strain WTC016 for nattokinase production. Fermentation-Basel 5, https://doi.org/10.3390/fermentation5040092 (2019).

  • 98.

    Mouloud, G., Daoud, H., Bassem, J., Atef, I. & Hani, B. New bacteriocin from Bacillus clausii strainGM17: purification, characterization, and biological activity. Appl. Biochem. Biotech. 171, 2186–2200 (2013).

    CAS 

    Google Scholar 


  • Source: Ecology - nature.com

    Bringing climate reporting to local newsrooms

    Cryofouling avoidance in the Antarctic scallop Adamussium colbecki