Abstract
The draft genome sequence and main genomic features of Penicillium pancosmium MUM 23.27, isolated from Portuguese raw honey are reported. The genome size is 34.82 Mb, containing a 48.99% GC content, 11,394 genes, with 39 rRNAs and 147 tRNAs/tmRNAs. Twenty-six BGCs were predicted with four exhibiting significant similarities with YWA1, chaetoglobosin A/chaetoglobosin C, squalestatin S1, and nidulanin A. Moreover, the whole-genome sequencing and in silico genomic analysis, allowed to further understand some aspects of this species habitat, resistance, and evolutionary genomic events. Altogether, the results obtained also allow to dwell deeper on particular Penicillia biological characteristics and genomic traits, permitting them to thrive in these honey substrates. In addition, this resource represents the first genome for the species and one of the first for raw honeys filamentous fungi.
References
Baldrian P, Valásková V (2008) Degradation of cellulose by basidiomycetous fungi. F Mic Rev 32:501–521. https://doi.org/10.1111/j.1574-6976.2008.00106.x
Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Com Bio 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Bignell E, Cairns TC, Throckmorton K et al (2016) Secondary metabolite arsenal of an opportunistic pathogenic fungus. Philos Trans R Soc B Biol Sci 371:20160023. https://doi.org/10.1098/rstb.2016.0023
Blin K, Shaw S, Kloosterman AM et al (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nuc Aci Res 49:W29–W35. https://doi.org/10.1093/nar/gkab335
Blum M, Chang H-Y, Chuguransky S et al (2021) The InterPro protein families and domains database: 20 years on. Nucl Acids Res 49:D344–D354. https://doi.org/10.1093/nar/gkaa977
Bogdanov S (2016) Honey as Nutrient and Functional Food. In: Book of Honey. Bee Product Science 19, pp 1-47
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Met 12:59–60. https://doi.org/10.1038/nmeth.3176
Cantalapiedra CP, Hernández-Plaza A, Letunic I et al (2021) eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Bio Evo 38:5825–5829. https://doi.org/10.1093/molbev/msab293
Carvalho M, Estevinho LM, Choupina A (2010) Yeast species associated with honey: different identification methods. Arc Zoo 59:103–113
Cheng M, Zhao S, Liu H et al (2021) Functional analysis of a chaetoglobosin A biosynthetic regulator in Chaetomium globosum. Fun Bio 125:201–210. https://doi.org/10.1016/j.funbio.2020.10.010
Coleine C, Masonjones S, Sterflinger K et al (2020) Peculiar genomic traits in the stress-adapted cryptoendolithic Antarctic fungus Friedmanniomyces endolithicus. Fun Bio 124:458–467. https://doi.org/10.1016/j.funbio.2020.01.005
Conesa A, Götz S, García-Gómez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. https://doi.org/10.1093/bioinformatics/bti610
de Vries RP, Riley R, Wiebenga A et al (2017) Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus. Gen Bio 18:28. https://doi.org/10.1186/s13059-017-1151-0
Edler D, Klein J, Antonelli A, Silvestro D (2021) raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Met Eco Evo 12:373–377. https://doi.org/10.1111/2041-210X.13512
Felšöciová S, Kačániová M, Hleba L et al (2012) Microscopic fungi isolated from Polish honey. J Microbiol Biotechnol Food Sci 3:1040–1049
Fujii I, Yasuoka Y, Tsai H-F et al (2004) Hydrolytic Polyketide Shortening by Ayg1p, a Novel Enzyme Involved in Fungal Melanin Biosynthesis. J Bio Che 279:44613–44620. https://doi.org/10.1074/jbc.M406758200
Götz S, García-Gómez JM, Terol J et al (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nuc Aci Res 36:3420–3435. https://doi.org/10.1093/nar/gkn176
Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075. https://doi.org/10.1093/bioinformatics/btt086
Hawksworth DL, Wiltshire P (2015) Forensic mycology: current perspectives. Res Rep for Med Sci. https://doi.org/10.2147/RRFMS.S83169
Hoffmeister D, Keller NP (2007) Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat pro Rep 24:393–416. https://doi.org/10.1039/B603084J
Houbraken J, Kocsubé S, Visagie CM et al (2020) Classification of Aspergillus, Penicillium, Talaromyces and related genera (Eurotiales): An overview of families, genera, subgenera, sections, series and species. Stu Myc 95:5–169. https://doi.org/10.1016/j.simyco.2020.05.002
Houbraken J, Visagie CM, Frisvad JC (2021) Recommendations to prevent taxonomic misidentification of genome-sequenced fungal strains. Mic Res Ann 10:e01074-e1120. https://doi.org/10.1128/MRA.01074-20
Jalili V, Afgan E, Gu Q et al (2020) The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2020 update. Nuc Aci Res 48:W395–W402. https://doi.org/10.1093/nar/gkaa434
Jones P, Binns D, Chang H-Y et al (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240. https://doi.org/10.1093/bioinformatics/btu031
Jurado V, Del Rosal Y, Liñan C et al (2021) Diversity and seasonal dynamics of airborne fungi in Nerja Cave. Spain App Sci 11:6236. https://doi.org/10.3390/app11136236
Kacániová K, Pavlicová P et al (2009) Microbial communities in bees, pollen and honey from Slovakia. Acta Mic Imm Hun 56:285–295. https://doi.org/10.1556/AMicr.56.2009.3.7
Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Bio 428:726–731. https://doi.org/10.1016/j.jmb.2015.11.006
Katoh K, Standley DM (2013) MAFFT Multiple sequence alignment software Version 7: improvements in performance and usability. Mol Bio Evo 30:772–780. https://doi.org/10.1093/molbev/mst010
Kriventseva EV, Kuznetsov D, Tegenfeldt F et al (2019) OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nuc Aci Res 47:D807–D811. https://doi.org/10.1093/nar/gky1053
Laslett D, Canback B (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nuc Aci Res 32:11–16. https://doi.org/10.1093/nar/gkh152
Li L, Stoeckert CJ, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Gen Res 13:2178–2189. https://doi.org/10.1101/gr.1224503
Mack J (2022) The Biodiversity of Microfungi Isolated from the Bark of the Sugar Maple (Acer saccharum). Carleton University, Master of Science
Martínez AT, Speranza M, Ruiz-Dueñas FJ et al (2005) Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8:195–204
Martins HM, Martins ML, Bernardo FMA (2003) Bacillaceae spores, fungi and aflatoxins determination in honey Esporos de Bacillaceae, fungos e aflatoxinas em mel. Rev Por Cie Vet 98:85–88
Mendes FK, Vanderpool D, Fulton B, Hahn MW (2020) CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics 36(22–23):5516–5518. https://doi.org/10.1093/bioinformatics/btaa1022
Obersteiner A, Gilles S, Frank U et al (2016) Pollen-associated microbiome correlates with pollution parameters and the allergenicity of pollen. PLoS ONE 11:e0149545. https://doi.org/10.1371/journal.pone.0149545
Pao SS, Paulsen IT, Saier MH (1998) Major Facilitator Superfamily Mol Bio Rev 62:1–34. https://doi.org/10.1128/MMBR.62.1.1-34.1998
Petersen C, Sørensen T, Nielsen MR et al (2023) Comparative genomic study of the Penicillium genus elucidates a diverse pangenome and 15 lateral gene transfer events. Int Myc Ass Fun 14:3. https://doi.org/10.1186/s43008-023-00108-7
Piras M, Patruno I, Nikolakopoulou C et al (2021) Synthesis of the fungal metabolite YWA1 and related constructs as tools to study MelLec-mediated immune response to aspergillus infections. J Org Che 86:6044–6055. https://doi.org/10.1021/acs.joc.0c02324
Pitt JI, Hocking AD (2022) Fungi and Food Spoilage. Springer International Publishing, Cham
Price MN, Dehal PS, Arkin AP (2010) FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. https://doi.org/10.1371/journal.pone.0009490
Rokas A, Mead ME, Steenwyk JL et al (2020) Biosynthetic gene clusters and the evolution of fungal chemodiversity. Nat pro Rep 37:868–878. https://doi.org/10.1039/C9NP00045C
Roxo I, Amaral AL, Portugal A et al (2023) A checklist of fungi isolated from honey (2000–2022). Stu Fun 8:14. https://doi.org/10.48130/SIF-2023-0014
Roxo I (2023) Exploring the fungal diversity in Portuguese honey. M.Sc. Thesis, Instituto Superior de Engenharia de Coimbra
Seemann T (2013) Barrnap 0.7: rapid ribosomal RNA prediction
Simão FA, Waterhouse RM, Ioannidis P et al (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212. https://doi.org/10.1093/bioinformatics/btv351
Sirithep K, Xiao F, Raethong N et al (2020) Probing carbon utilization of cordyceps militaris by sugar transportome and protein structural analysis. Cells 9:401. https://doi.org/10.3390/cells9020401
Stanke M, Morgenstern B (2005) AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nuc Aci Res 33:W465–W467. https://doi.org/10.1093/nar/gki458
Sun J, Lu F, Luo Y et al (2023) OrthoVenn3: an integrated platform for exploring and visualizing orthologous data across genomes. Nuc Aci Res 51:W397–W403. https://doi.org/10.1093/nar/gkad313
Teixeira MM, Moreno LF, Stielow BJ et al (2017) Exploring the genomic diversity of black yeasts and relatives (Chaetothyriales, Ascomycota). Stu Myc 86:1–28. https://doi.org/10.1016/j.simyco.2017.01.001
The UniProt Consortium (2017) UniProt: the universal protein knowledgebase. Nuc Aci Res 45:D158–D169. https://doi.org/10.1093/nar/gkw1099
Visagie CM, Hirooka Y, Tanney JB et al (2014a) Aspergillus, Penicillium and Talaromyces isolated from house dust samples collected around the world. Stu Myc 78:63–139. https://doi.org/10.1016/j.simyco.2014.07.002
Visagie CM, Houbraken J, Frisvad JC et al (2014b) Identification and nomenclature of the genus Penicillium. Stu Myc 78:343–371. https://doi.org/10.1016/j.simyco.2014.09.001
Zheng J, Ge Q, Yan Y et al (2023) dbCAN3: automated carbohydrate-active enzyme and substrate annotation. Nuc Aci Res 51:W115–W121. https://doi.org/10.1093/nar/gkad328
Zucconi L, Canini F, Isola D, Caneva G (2022) Fungi affecting wall paintings of historical value: a worldwide meta-analysis of their detected diversity. App Sci 12:2988. https://doi.org/10.3390/app12062988
Acknowledgements
We are grateful to Genoinseq (Cantanhede, Portugal) and IBIMED (Aveiro, Portugal) for the help with the genome sequencing.
Funding
This work was partially carried out in the R&D Unit Centre for Functional Ecology –Science for People & the Planet (CFE), with reference UIDB/04004/2020, and Associate Laboratory TERRA, with reference LA/P/0092/2020, financed by FCT/MCTES through national funds (PIDDAC).
Author information
Authors and Affiliations
Contributions
I.R. and J.T. wrote the main manuscript text. A.P and A. A. check all the cientific anotations. All authors reviewed the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Yusuf Akhter.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Roxo, I., Amaral, A., Portugal, A. et al. Draft genome sequence and comparative genomic analysis of Penicillium pancosmium MUM 23.27 isolated from raw honey. Arch Microbiol 206, 36 (2024). https://doi.org/10.1007/s00203-023-03766-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-023-03766-8