The planctomycete Stieleria maiorica Mal15


Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
12 06 2020
Historique:
received: 15 01 2019
accepted: 30 04 2020
entrez: 14 6 2020
pubmed: 14 6 2020
medline: 16 6 2021
Statut: epublish

Résumé

Bacterial strains of the phylum Planctomycetes occur ubiquitously, but are often found on surfaces of aquatic phototrophs, e.g. alga. Despite slower growth, planctomycetes are not outcompeted by faster-growing bacteria in biofilms on such surfaces; however, strategies allowing them to compensate for slower growth have not yet been investigated. Here, we identified stieleriacines, a class of N-acylated tyrosines produced by the novel planctomycete Stieleria maiorica Mal15

Identifiants

pubmed: 32533057
doi: 10.1038/s42003-020-0993-2
pii: 10.1038/s42003-020-0993-2
pmc: PMC7293339
doi:

Substances chimiques

Anti-Bacterial Agents 0
Tyrosine 42HK56048U

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

303

Commentaires et corrections

Type : ErratumIn
Type : ErratumIn

Références

Kohn, T. et al. Planctopirus ephydatiae, a novel Planctomycete isolated from a freshwater sponge. Syst. Appl. Microbiol. 43, 126022 (2019).
pubmed: 31785948 doi: 10.1016/j.syapm.2019.126022 pmcid: 31785948
Lage, O. M. & Bondoso, J. Planctomycetes and macroalgae, a striking association. Front. Microbiol. 5, 267 (2014).
pubmed: 24917860 pmcid: 4042473 doi: 10.3389/fmicb.2014.00267
Frank, O. et al. Plasmid curing and the loss of grip—the 65-kb replicon of Phaeobacter inhibens DSM 17395 is required for biofilm formation, motility and the colonization of marine algae. Syst. Appl. Microbiol. 38, 120–127 (2014).
pubmed: 25595869 doi: 10.1016/j.syapm.2014.12.001 pmcid: 25595869
Van Wagoner, R. M. & Clardy, J. FeeM, an N-acyl amino acid synthase from an uncultured soil microbe: structure, mechanism, and acyl carrier protein binding. Structure 14, 1425–1435 (2006).
pubmed: 16962973 doi: 10.1016/j.str.2006.07.005 pmcid: 16962973
Whiteley, M., Diggle, S. P. & Greenberg, E. P. Progress in and promise of bacterial quorum sensing research. Nature 551, 313–320 (2017).
pubmed: 29144467 pmcid: 5870893 doi: 10.1038/nature24624
Papenfort, K. & Bassler, B. L. Quorum sensing signal-response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14, 576–588 (2016).
pubmed: 27510864 pmcid: 5056591 doi: 10.1038/nrmicro.2016.89
Wiegand, S., Jogler, M. & Jogler, C. On the maverick planctomycetes. FEMS Microbiol. Rev. 42, 739–760 (2018).
pubmed: 30052954 doi: 10.1093/femsre/fuy029 pmcid: 30052954
Frank, C. S., Langhammer, P., Fuchs, B. M. & Harder, J. Ammonium and attachment of Rhodopirellula baltica. Arch. Microbiol. 193, 365–372 (2011).
pubmed: 21340506 pmcid: 21340506
Waters, C. M. & Bassler, B. L. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319–346 (2005).
pubmed: 16212498 doi: 10.1146/annurev.cellbio.21.012704.131001 pmcid: 16212498
Wiegand, S. et al. Cultivation and functional characterization of 79 planctomycetes uncovers their unique biology. Nat. Microbiol. 5, 126–140 (2020).
pubmed: 31740763 doi: 10.1038/s41564-019-0588-1 pmcid: 31740763
Jeske, O., Jogler, M., Petersen, J., Sikorski, J. & Jogler, C. From genome mining to phenotypic microarrays: planctomycetes as source for novel bioactive molecules. Antonie Van. Leeuwenhoek 104, 551–567 (2013).
pubmed: 23982431 doi: 10.1007/s10482-013-0007-1 pmcid: 23982431
Clardy, J. & Brady, S. F. Cyclic AMP directly activates NasP, an N-acyl amino acid antibiotic biosynthetic enzyme cloned from an uncultured beta-proteobacterium. J. Bacteriol. 189, 6487–6489 (2007).
pubmed: 17586635 pmcid: 1951892 doi: 10.1128/JB.00457-07
Thies, S. et al. Metagenomic discovery of novel enzymes and biosurfactants in a slaughterhouse biofilm microbial community. Sci. Rep. 6, 27035 (2016).
pubmed: 27271534 pmcid: 4897644 doi: 10.1038/srep27035
Brady, S. F., Clardy, J. & Long-Chain N-Acyl amino acid antibiotics isolated from heterologously expressed environmental DNA. J. Am. Chem. Soc. 122, 12903–12904 (2000).
doi: 10.1021/ja002990u
Brady, S. F., Chao, C. J., Clardy, J. & Long-chain N-acyltyrosine synthases from environmental DNA. Appl. Environ. Microbiol. 70, 6865–6870 (2004).
pubmed: 15528554 pmcid: 525126 doi: 10.1128/AEM.70.11.6865-6870.2004
Brady, S. F. & Clardy, J. N-acyl derivatives of arginine and tryptophan isolated from environmental DNA expressed in Escherichia coli. Org. Lett. 7, 3613–3616 (2005).
pubmed: 16092832 doi: 10.1021/ol0509585 pmcid: 16092832
Brady, S. F., Chao, C. J. & Clardy, J. New natural product families from an environmental DNA (eDNA) gene cluster. J. Am. Chem. Soc. 124, 9968–9969 (2002).
pubmed: 12188643 doi: 10.1021/ja0268985 pmcid: 12188643
Deering, R. W. et al. N-acyl dehydrotyrosines, tyrosinase inhibitors from the marine bacterium Thalassotalea sp. PP2-459. J. Nat. Prod. 79, 447–450 (2016).
pubmed: 26824128 pmcid: 5821419 doi: 10.1021/acs.jnatprod.5b00972
Morris, R., Longnecker, K. & Giovannoni, S. Pirellula and OM43 are among the dominant lineages identified in an Oregon coast diatom bloom. Environ. Microbiol. 8, 1361–1370 (2006).
pubmed: 16872400 doi: 10.1111/j.1462-2920.2006.01029.x pmcid: 16872400
Hengst, M. B., Andrade, S., González, B. & Correa, J. A. Changes in epiphytic bacterial communities of intertidal seaweeds modulated by host, temporality, and copper enrichment. Microb. Ecol. 60, 282–290 (2010).
pubmed: 20333374 doi: 10.1007/s00248-010-9647-0 pmcid: 20333374
Zan, J., Liu, Y., Fuqua, C. & Hill, R. T. Acyl-homoserine lactone quorum sensing in the Roseobacter clade. Int. J. Mol. Sci. 15, 654–669 (2014).
pubmed: 24402124 pmcid: 3907830 doi: 10.3390/ijms15010654
Wilson, M. Z., Wang, R., Gitai, Z. & Seyedsayamdost, M. R. Mode of action and resistance studies unveil new roles for tropodithietic acid as an anticancer agent and the γ-glutamyl cycle as a proton sink. Proc. Natl Acad. Sci. USA 113, 1630–1635 (2016).
pubmed: 26802120 doi: 10.1073/pnas.1518034113 pmcid: 26802120
Berger, M., Neumann, A., Schulz, S., Simon, M. & Brinkhoff, T. Tropodithietic acid production in Phaeobacter gallaeciensis is regulated by N-acyl homoserine lactone-mediated quorum sensing. J. Bacteriol. 193, 6576–6585 (2011).
pubmed: 21949069 pmcid: 3232910 doi: 10.1128/JB.05818-11
Beyersmann, P. G. et al. Dual function of tropodithietic acid as antibiotic and signaling molecule in global gene regulation of the probiotic bacterium Phaeobacter inhibens. Sci. Rep. 7, 730 (2017).
pubmed: 28389641 pmcid: 5429656 doi: 10.1038/s41598-017-00784-7
Will, S. E. et al. The limits to growth—energetic burden of the endogenous antibiotic tropodithietic acid in Phaeobacter inhibens DSM 17395. PLoS ONE 12, e0177295 (2017).
pubmed: 28481933 pmcid: 5421792 doi: 10.1371/journal.pone.0177295
MacIntyre, L. W., Charles, M. J., Haltli, B. A., Marchbank, D. H. & Kerr, R. G. An Ichip-domesticated sponge bacterium produces an N-acyltyrosine bearing an α-methyl substituent. Org. Lett. 21, 7768–7771 (2019).
pubmed: 31524403 doi: 10.1021/acs.orglett.9b02710 pmcid: 31524403
Lee, C.-M. et al. Characterization of a novel antibacterial N-acyl amino acid synthase from soil metagenome. J. Biotechnol. 294, 19–25 (2019).
pubmed: 30771442 doi: 10.1016/j.jbiotec.2019.01.017 pmcid: 30771442
Li, L. et al. Characterization of the saframycin A gene cluster from Streptomyces lavendulae NRRL 11002 revealing a nonribosomal peptide synthetase system for assembling the unusual tetrapeptidyl skeleton in an iterative manner. J. Bacteriol. 190, 251–263 (2008).
pubmed: 17981978 pmcid: 2223732 doi: 10.1128/JB.00826-07
Craig, J. W., Cherry, M. A. & Brady, S. F. Long-chain N-acyl amino acid synthases are linked to the putative PEP-CTERM/exosortase protein-sorting system in Gram-negative bacteria. J. Bacteriol. 193, 5707–5715 (2011).
pubmed: 21840974 pmcid: 3187218 doi: 10.1128/JB.05426-11
Taresco, V. et al. New N-acyl amino acid-functionalized biodegradable polyesters for pharmaceutical and biomedical applications. RSC Adv. 6, 109401–109405 (2016).
doi: 10.1039/C6RA21464A
Joondan, N., Jhaumeer‐Laulloo, S., Caumul, P. & Akerman, M. Synthesis, physicochemical, and biological activities of novel N‐acyl tyrosine monomeric and gemini surfactants in single and SDS/CTAB–mixed micellar system. J. Phys. Org. Chem. 30, e3675 (2017).
doi: 10.1002/poc.3675
Jeske, O. et al. Developing techniques for the utilization of planctomycetes as producers of bioactive molecules. Front. Microbiol. 7, 1242 (2016).
pubmed: 27594849 pmcid: 4990742 doi: 10.3389/fmicb.2016.01242
Kohn, T. et al. Fuerstia marisgermanicae gen. nov., sp. nov., an unusual member of the phylum planctomycetes from the German Wadden Sea. Front. Microbiol 7, 2079 (2016).
pubmed: 28066393 pmcid: 5177795 doi: 10.3389/fmicb.2016.02079
Kohn, T. et al. Corrigendum: Fuerstia marisgermanicae gen. nov., sp. nov., an unusual member of the phylum planctomycetes from the German Wadden Sea. Front. Microbiol. 10, 1029 (2019).
pubmed: 31156577 pmcid: 6529766 doi: 10.3389/fmicb.2019.01029
Rast, P. et al. Three novel species with peptidoglycan cell walls form the new genus Lacunisphaera gen. nov. in the family Opitutaceae of the verrucomicrobial subdivision 4. Front. Microbiol. 8, 202 (2017).
pubmed: 28243229 pmcid: 5303756 doi: 10.3389/fmicb.2017.00202
Kallscheuer, N. et al. Description of three bacterial strains belonging to the new genus Novipirellula gen. nov., reclassificiation of Rhodopirellula rosea and Rhodopirellula caenicola and readjustment of the genus threshold of the phylogenetic marker rpoB for Planctomycetaceae. Antonie van Leeuwenhoek https://doi.org/10.1007/s10482-019-01374-51-17 (2019).
Boersma, A. et al. Alienimonas californiensis gen. nov. sp. nov., a novel planctomycete isolated from the kelp forest in Monterey Bay. Antonie van Leeuwenhoek. https://doi.org/10.1007/s10482-019-01367-4 (2019).
Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012).
pubmed: 22556368 pmcid: 3389763 doi: 10.1093/bioinformatics/bts252
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
pubmed: 24451623 pmcid: 24451623 doi: 10.1093/bioinformatics/btu033
Lechner, M. et al. Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinform. 12, 124 (2011).
doi: 10.1186/1471-2105-12-124
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147 pmcid: 390337 doi: 10.1093/nar/gkh340
Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000).
pubmed: 10742046 pmcid: 10742046 doi: 10.1093/oxfordjournals.molbev.a026334
Lee, I., Ouk Kim, Y., Park, S. C. & Chun, J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol. 66, 1100–1103 (2016).
pubmed: 26585518 doi: 10.1099/ijsem.0.000760 pmcid: 26585518
Rodriguez-R, L. M. & Konstantinidis, K. T. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Prepr. 4, e1900v1 (2016).
Qin, Q.-L. et al. A proposed genus boundary for the prokaryotes based on genomic insights. J. Bacteriol. 196, 2210–2215 (2014).
pubmed: 24706738 pmcid: 4054180 doi: 10.1128/JB.01688-14
Bondoso, J., Harder, J. & Lage, O. M. rpoB gene as a novel molecular marker to infer phylogeny in Planctomycetales. Antonie Van. Leeuwenhoek 104, 477–488 (2013).
pubmed: 23904187 doi: 10.1007/s10482-013-9980-7 pmcid: 23904187
Sievers, F. et al. Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
pubmed: 21988835 pmcid: 3261699 doi: 10.1038/msb.2011.75
Surup, F. et al. Deconins A–E: cuparenic and mevalonic or propionic acid conjugates from the basidiomycete Deconica sp. 471. J. Nat. Prod. 78, 934–938 (2015).
pubmed: 25871540 doi: 10.1021/np5010104 pmcid: 25871540
Boedeker, C. et al. Determining the bacterial cell biology of planctomycetes. Nat. Commun. 8, 14853 (2017).
pubmed: 28393831 pmcid: 5394234 doi: 10.1038/ncomms14853
O’Toole, G. A. & Kolter, R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28, 449–461 (1998).
pubmed: 9632250 doi: 10.1046/j.1365-2958.1998.00797.x pmcid: 9632250

Auteurs

Nicolai Kallscheuer (N)

Department of Microbiology, Radboud University, Nijmegen, The Netherlands.

Olga Jeske (O)

Department of Microbiology, Radboud University, Nijmegen, The Netherlands.
Leibniz Institute DSMZ, Braunschweig, Germany.

Birthe Sandargo (B)

Helmholtz Centre for Infection Research, Braunschweig, Germany.
German Centre for Infection Research (DZIF), Braunschweig, Germany.

Christian Boedeker (C)

Leibniz Institute DSMZ, Braunschweig, Germany.

Sandra Wiegand (S)

Department of Microbiology, Radboud University, Nijmegen, The Netherlands.
Institute for Biological Interfaces 5, Karlsruhe Institute of Technology, Eggenstein-Leopoldshafen, Germany.

Pascal Bartling (P)

Leibniz Institute DSMZ, Braunschweig, Germany.

Mareike Jogler (M)

Leibniz Institute DSMZ, Braunschweig, Germany.

Manfred Rohde (M)

Central Facility for Microscopy, Helmholtz Centre for Infection Research, Braunschweig, Germany.

Jörn Petersen (J)

Leibniz Institute DSMZ, Braunschweig, Germany.

Marnix H Medema (MH)

Bioinformatics Group, Wageningen University, Wageningen, The Netherlands.

Frank Surup (F)

Helmholtz Centre for Infection Research, Braunschweig, Germany. Frank.Surup@helmholtz-hzi.de.
German Centre for Infection Research (DZIF), Braunschweig, Germany. Frank.Surup@helmholtz-hzi.de.

Christian Jogler (C)

Department of Microbiology, Radboud University, Nijmegen, The Netherlands. Christian@Jogler.de.
Department of Microbial Interactions, Friedrich-Schiller University, Jena, Germany. Christian@Jogler.de.

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