Abstract
Janthinobacterium agaricidamnosum causes soft-rot disease of the cultured button mushroom Agaricus bisporus and is thus responsible for agricultural losses. Here, we present the genome sequence of J. agaricidamnosum DSM 9628. The 5.9-Mb genome harbors several secondary metabolite biosynthesis gene clusters, which renders this neglected bacterium a promising source for genome mining approaches.
GENOME ANNOUNCEMENT
The soft-rot disease of the cultured button mushroom Agaricus bisporus results from an infection with the Gram-negative bacterium Janthinobacterium agaricidamnosum (1). Despite its devastating disease outcome that accounts for substantial losses in agriculture, the pathobiology of the soft-rot disease has not been investigated in the past. Recently, we discovered that the cyclic lipopeptide jagaricin is involved in the soft-rot infection process (2). Moreover, jagaricin exhibits strong antifungal activity against major human pathogenic fungi (2).
The genome of J. agaricidamnosum DSM 9628 was sequenced using the 454 GS FLX Titanium system (282,254 reads) with an 8-kb paired-end library (405,849 reads) to a 24-fold coverage. The Newbler assembler (454 Life Science) was used for assembly of the sequencing reads. 167 contigs (N50 contig size 113,797 bp) were assembled into 9 scaffolds (N50 scaffold size 595,787 bp). Gene annotation was carried out by the IGS (Institute for Genome Science, University of Maryland, School of Medicine) prokaryotic annotation platform (3). The genome of J. agaricidamnosum has a total size of 5,949,001 bp, has an overall G+C content of 61%, and consists of 5,573 open reading frames, of which 4,327 (77.6%) were assigned a biological function.
In addition to the characterized jagaricin biosynthesis gene cluster (2), whole-genome sequencing of J. agaricidamnosum revealed a gene locus for violacein production (2, 4, 5) as well as several orphan natural product biosynthesis gene clusters: Three gene clusters coding for nonribosomal peptide synthetases (NRPSs), one hybrid NRPS-polyketide synthase (PKS) gene cluster, one putative siderophore biosynthesis gene cluster, and one bacteriocin biosynthesis gene cluster. This genome analysis highlights that such neglected bacteria can be a hidden source for novel secondary metabolites (6).
To date, seven genomes of Janthinobacterium spp. are accessible by the DDBJ/EMBL/GenBank databases, and five of them have been published (7–11). However, J. agaricidamnosum is the first pathogenic Janthinobacterium that has been sequenced. The other Janthinobacterium spp. sequenced so far have been isolated from water, glaciers, soil, and rhizosphere.
Insight into the genome of J. agaricidamnosum not only reveals a high potential to produce secondary metabolites, but it could also aid in investigating the mechanism of soft-rot infection.
Nucleotide sequence accession number.
The genome sequence of J. agaricidamnosum has been deposited in DDBJ/EMBL/GenBank under the accession no. HG322949. The version described in this paper is the first version.
ACKNOWLEDGMENTS
We thank the Institute for Genome Science (University of Maryland, School of Medicine) for kindly providing the IGS prokaryotic annotation service.
This research was supported by the International Leibniz Research School for Microbial and Biomolecular Interactions (ILRS) as part of the excellence graduate school Jena School for Microbial Communication (JSMC).
Footnotes
Citation Graupner K, Lackner G, Hertweck C. 2015. Genome sequence of mushroom soft-rot pathogen Janthinobacterium agaricidamnosum. Genome Announc 3(2):e00277-15. doi:10.1128/genomeA.00277-15.
REFERENCES
- 1.Lincoln SP, Fermor TR, Tindall BJ. 1999. Janthinobacterium agaricidamnosum sp. nov., a soft rot pathogen of Agaricus bisporus. Int J Syst Bacteriol 49:1577–1589. doi: 10.1099/00207713-49-4-1577. [DOI] [PubMed] [Google Scholar]
- 2.Graupner K, Scherlach K, Bretschneider T, Lackner G, Roth M, Gross H, Hertweck C. 2012. Imaging mass spectrometry and genome mining reveal highly antifungal virulence factor of mushroom soft rot pathogen. Angew Chem Int Ed Engl 51:13173–13177. doi: 10.1002/anie.201206658. [DOI] [PubMed] [Google Scholar]
- 3.Galens K, Orvis J, Daugherty S, Creasy HH, Angiuoli S, White O, Wortman J, Mahurkar A, Giglio MG. 2011. The IGS standard operating procedure for automated prokaryotic annotation. Stand Genomic Sci 4:244–251. doi: 10.4056/sigs.1223234. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.August PR, Grossman TH, Minor C, Draper MP, MacNeil IA, Pemberton JM, Call KM, Holt D, Osburne MS. 2000. Sequence analysis and functional characterization of the violacein biosynthetic pathway from Chromobacterium violaceum. J Mol Microbiol Biotechnol 2:513–519. [PubMed] [Google Scholar]
- 5.Sánchez C, Braña AF, Méndez C, Salas JA. 2006. Reevaluation of the violacein biosynthetic pathway and its relationship to indolocarbazole biosynthesis. Chembiochem 7:1231–1240. doi: 10.1002/cbic.200600029. [DOI] [PubMed] [Google Scholar]
- 6.Pidot SJ, Coyne S, Kloss F, Hertweck C. 2014. Antibiotics from neglected bacterial sources. Int J Med Microbiol 304:14–22. doi: 10.1016/j.ijmm.2013.08.011. [DOI] [PubMed] [Google Scholar]
- 7.Hornung C, Poehlein A, Haack FS, Schmidt M, Dierking K, Pohlen A, Schulenburg H, Blokesch M, Plener L, Jung K, Bonge A, Krohn-Molt I, Utpatel C, Timmermann G, Spieck E, Pommerening-Röser A, Bode E, Bode HB, Daniel R, Schmeisser C, Streit WR. 2013. The Janthinobacterium sp. HH01 genome encodes a homologue of the V. cholerae CqsA and L. pneumophila LqsA autoinducer synthases. PLoS One 8:e55045. doi: 10.1371/journal.pone.0055045. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Kim SJ, Shin SC, Hong SG, Lee YM, Lee H, Lee J, Choi IG, Park H. 2012. Genome sequence of Janthinobacterium sp. strain PAMC 25724, isolated from alpine glacier cryoconite. J Bacteriol 194:2096. doi: 10.1128/JB.00096-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Smith H, Akiyama T, Foreman C, Franklin M, Woyke T, Teshima H, Davenport K, Daligault H, Erkkila T, Goodwin L, Gu W, Xu Y, Chain P. 2013. Draft genome sequence and description of Janthinobacterium sp. strain CG3, a psychrotolerant Antarctic supraglacial stream bacterium. Genome Announc 1(6):e00960-13. doi: 10.1128/genomeA.00960-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Audic S, Robert C, Campagna B, Parinello H, Claverie JM, Raoult D, Drancourt M. 2007. Genome analysis of Minibacterium massiliensis highlights the convergent evolution of water-living bacteria. PLoS Genet 3:e138. doi: 10.1371/journal.pgen.0030138. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.McTaggart TL, Shapiro N, Woyke T, Chistoserdova L. 2015. Draft genome of Janthinobacterium sp. RA13 isolated from Lake Washington sediment. Genome Announc 3(1):e01588-14. doi: 10.1128/genomeA.01588-14. [DOI] [PMC free article] [PubMed] [Google Scholar]