Lau, SKP

Tam, WT

TSANG, CC

Woo, PCY

Mitochondrial DNA Part B

HKU Scholars Hub

TitleComparative mitogenomic and phylogenetic characterization onthe complete mitogenomes of Talaromyces(Penicillium) marneffeiAuthor(s) Tam, WT; TSANG, CC; Lau, SKP; Woo, PCYCitation Mitochondrial DNA Part B, 2016, v. 1 n. 1, p. 941-942Issued Date 2016URL http://hdl.handle.net/10722/237769RightsPREPRINTThis is a preprint of an article whose final and definitive form hasbeen published in the[JOURNAL TITLE] [year of publication] [copyright Taylor &Francis]; [JOURNAL TITLE] isavailable online at: http://www.informaworld.com/smpp/ with theopen URL of your articlePOSTPRINTThis is an Accepted Manuscript of an article published by Taylor& Francis in [JOURNAL TITLE] on [date of publication], availableonline: http://wwww.tandfonline.com/[Article DOI]; This work islicensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.MITOGENOME ANNOUNCEMENTComparative mitogenomic and phylogenetic characterization on the completemitogenomes of Talaromyces (Penicillium) marneffeiEmily W. T. Tama, Chi-Ching Tsanga , Susanna K. P. Laua,b,c,d,e and Patrick C. Y. Wooa,b,c,d,eaDepartment of Microbiology, The University of Hong Kong, Hong Kong; bState Key Laboratory of Emerging Infectious Diseases, TheUniversity of Hong Kong, Hong Kong; cResearch Centre of Infection and Immunology, The University of Hong Kong, Hong Kong; dCarol YuCentre of Infection, The University of Hong Kong, Hong Kong; eCollaborative Innovation Center for Diagnosis and Treatment of InfectiousDiseases, The University of Hong Kong, Hong KongABSTRACTWe report the complete mitochondrial DNA (mtDNA) sequences of four Talaromyces marneffei strainsand performed comparative genomic and phylogenetic analyses. The gene orders of the four mtDNAsare identical to the previously published mtDNA of strain PM1 (nad4l, nad5, nad2, atp9, cob, nad1,nad4, atp8, atp6, nad6, cox3, rps, cox1, nad3, cox2). Phylogenetic analysis showed that the four mtDNAswere clustered with that of PM1 with high bootstrap support. Compared to mtDNA of PM1, the onlynon-synonymous mutation was located in nad2 (T505M) of strain PM26. Synonymous single nucleotidepolymorphisms were observed at eight positions in the four mtDNAs.ARTICLE HISTORYReceived 4 November 2016Accepted 14 November 2016KEYWORDSMitogenome; Talaromycesmarneffei; Penicilliummarneffei; phylogeny;comparative genomicsTalaromyces (Penicillium) marneffei is the most important ther-mally dimorphic, systemic mycosis-causing fungus inSoutheast Asia (Vanittanakom et al. 2006). Apart from beingan AIDS-defining condition, penicilliosis has also beenreported in other immunocompromised patients (Chan et al.2016). Recently, we have described the emergence of penicil-liosis in patients on anti-CD20 monoclonal antibodies or kin-ase inhibitors (Chan et al. 2015). In 2003, we reported thecomplete mitochondrial DNA (mtDNA) sequence of T. marnef-fei strain PM1 (Woo et al. 2003). Subsequently, we havereported its draft genome sequence (Woo et al. 2011), sexualcycle-related genes (Woo et al. 2006), and polyketide syn-thase gene clusters (Woo et al. 2010). In this article, we reportthe complete mtDNA sequences of four additional T. marnef-fei strains (PM18, PM19, PM20, and PM26) and performedcomparative genomic and phylogenetic analyses. The fourstrains were isolated from penicilliosis patients in Hong Kong,and were deposited to the National Collection of PathogenicFungi (NCPF), UK (PM18¼NCPF 4320, PM19¼NCPF 4321,PM20¼NCPF 4322, and PM26¼NCPF 4323). Their mtDNAswere deposited in the International Nucleotide SequenceDatabases with accession numbers KU761329–KU761332.Talaromyces marneffei mtDNA was prepared from arthroco-nidia grown at 37 C and purified using the MitochondrialDNA Isolation Kit following manufacturer’s instructions(PromoKine, Heidelberg, Germany). The mtDNA was PCR-amplified using primers designed following the previouslypublished PM1–mtDNA sequence (Woo et al. 2003), and theamplified products were sequenced with an ABI PRISM 3130xlGenetic Analyzer (Applied Biosystems, Waltham, MA). Thesequences were assembled using CAP3 (Huang & Madan1999). Annotation was performed according to Woo et al.(2003). The four mtDNAs were aligned with the mtDNA ofPM1. Maximum-likelihood tree was reconstructed using MEGA7.0.14 (Kumar et al. 2016).The mtDNAs of the four T. marneffei strains are circularmolecules, with lengths of 35,420–35,436 bp and GþC con-tents of 24.6–25.1%. The gene orders of the four genomesare identical to that of PM1 (nad4l, nad5, nad2, atp9, cob,nad1, nad4, atp8, atp6, nad6, cox3, rps, cox1, nad3, cox2).63.6% of the four genomes are represented by structuralgenes (40.5% protein-coding exons, 5.9% tRNA genes, and17.3% rRNA genes), 8.8% by intergenic spacer, and 32.4% byintrons. They contain 15 genes encoding subunits of respira-tory chain complexes (cytochrome oxidase subunits I–III[cox1–cox3], apocytochrome b [cob], reduced nicotinamide-adenine dinucleotide-ubiquinone oxidoreductase subunits[nad1, nad2, nad3, nad4, nad4l, nad5, and nad6]), three ATPsynthase subunits (atp6, atp8, and atp9), and ribosomal pro-tein of the small ribosomal subunit (rps). Phylogenetic ana-lysis showed that the four mtDNAs were clustered with thatof PM1 with high bootstrap support (Figure 1). Compared toPM1 mtDNA, the only non-synonymous mutation was locatedin nad2 (T505M) of PM26. Synonymous single nucleotidepolymorphisms were observed in PM18 at T1088C, T506C,C9268T, T11060C, and C11845T located in nad5, cob, nad4,atp8, and atp6, respectively; in PM19 at C11845T located inatp6; in PM20 at G1674A located in nad2; and in PM26 atCONTACT Patrick C. Y. Woo pcywoo@hku.hk; Susanna K. P. Lau skplau@hku.hk Department of Microbiology, The University of Hong Kong, 4/F,University Pathology Building, Queen Mary Hospital, Hong Kong 2016 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use,distribution, and reproduction in any medium, provided the original work is properly cited.MITOCHONDRIAL DNA PART B: RESOURCES, 2016VOL. 1, NO. 1, 941–942http://dx.doi.org/10.1080/23802359.2016.1261610G29088A located in cox1. The four mtDNAs also encode 28tRNAs and the 23S and 16S rRNAs (rnl and rns).Disclosure statementThe authors report no conflicts of interest. The authors alone are respon-sible for the content and writing of the paper.FundingThis work was partly supported by the Health and Medical ResearchFund (Food and Health Bureau, the Government of the Hong KongSpecial Administrative Region, Hong Kong, under Grant HKM-15-M07[commissioned project]); the Strategic Research Theme Fund, TheUniversity of Hong Kong, Hong Kong; and the Croucher Senior MedicalResearch Fellowship, Croucher Foundation, Hong Kong.ORCIDChi-Ching Tsang http://orcid.org/0000-0001-6705-2866ReferencesChan JFW, Chan TSY, Gill H, Lam FYF, Trendell-Smith NJ, Sridhar S, Tse H,Lau SKP, Hung IFN, Yuen K-Y, et al. 2015. Disseminated infections withTalaromyces marneffei in non-AIDS patients given monoclonal antibod-ies against CD20 and kinase inhibitors. Emerg Infect Disease.21:1101–1106.Chan JFW, Lau SKP, Yuen K-Y, Woo PCY. 2016. Talaromyces (Penicillium)marneffei infection in non-HIV-infected patients. Emerg MicrobesInfect. 5:e19.Huang X, Madan A. 1999. CAP3: a DNA sequence assembly program.Genome Res. 9:868–877.Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular EvolutionaryGenetics Analysis Version 7.0 for bigger datasets. Mol Biol Evol.33:1870–1874.Vanittanakom N, Cooper CR, Fisher MC, Sirisanthana T. 2006. Penicilliummarneffei infection and recent advances in the epidemiology andmolecular biology aspects. Clin Microbiol Rev. 19:95–110.Woo PCY, Chong KTK, Tse H, Cai JJ, Lau CCY, Zhou AC, Lau SKP,Yuen K-Y. 2006. Genomic and experimental evidence for a potentialsexual cycle in the pathogenic thermal dimorphic fungus Penicilliummarneffei. FEBS Lett. 580:3409–3416.Woo PCY, Lau SKP, Liu B, Cai JJ, Chong KTK, Tse H, Kao RYT, Chan C-M,Chow W-N, Yuen K-Y. 2011. Draft genome sequence of Penicilliummarneffei strain PM1. Eukaryot Cell. 10:1740–1741.Woo PCY, Tam EWT, Chong KTK, Cai JJ, Tung ETK, Ngan AHY, Lau SKP,Yuen K-Y. 2010. High diversity of polyketide synthase genes and themelanin biosynthesis gene cluster in Penicillium marneffei. FEBS J.277:3750–3758.Woo PCY, Zhen H, Cai JJ, Yu J, Lau SKP, Wang J, Teng JLL, Wong SSY,Tse RH, Chen R, et al. 2003. The mitochondrial genome of the thermaldimorphic fungus Penicillium marneffei is more closely related to thoseof molds than yeasts. FEBS Lett. 555:469–477.Talaromycesmarneffei PM1 (AY347307)Talaromycesmarneffei PM26 (KU761331)Talaromycesmarneffei PM19 (KU761330)Talaromycesmarneffei PM20 (KU761331)Talaromycesmarneffei ATCC 18224T (JQ354997)Talaromycesmarneffei PM18 (KU761329)Talaromycesstipitatus ATCC 10500T(JQ354994)Aspergillus flavus TCM2014 (NC_026920)Aspergillus ustus 3.3904 (NC_025570)Aspergillus kawachii IFO 4308 (AP012272)Aspergillus niger N909 (NC_007445)Aspergillus tubingensis 0932 (NC_007597)Penicillium nordicum UASWS BFE487 (KR952336)Penicillium solitum 20-01 (NC_016187)Penicillium digitatum PHI26 (CM001645)Penicillium digitatum Pd1 (CM001644)Penicillium digitatum Pd01 (NC_015080)Penicillium roqueforti UASWS P1 (KR952335)10010010010010085721001001000.1Figure 1. Phylogenetic tree showing the relationship of Talaromyces marneffei strains PM18, PM19, PM20, and PM26 to other Aspergillus, Penicillium, andTalaromyces species. The tree was inferred from the concatenated mitochondrial gene (cox1, cox2, cox3, cob, nad1, nad2, nad3, nad4, nad4l, nad5, nad6, atp6, apt8,and atp9) sequence data by the maximum-likelihood method with the substitution model GTR (general time reversible model)þG (gamma-distributed rate vari-ation). The scale bar indicates the estimated number of substitutions per base. Numbers at nodes indicate levels of bootstrap support calculated from 1000 repli-cates. All names and accession numbers are given as cited in the International Nucleotide Sequence Databases.942 E. W. T. TAM ET AL.

Comparative mitogenomic and phylogenetic characterization on the complete mitogenomes of Talaromyces (Penicillium) marneffei

We report the complete mitochondrial DNA (mtDNA) sequences of four Talaromyces marneffei strains and performed comparative genomic and phylogenetic analyses. The gene orders of the four mtDNAs are identical to the previously published mtDNA of strain PM1 (nad4l, nad5, nad2, atp9, cob, nad1, nad4, atp8, atp6, nad6, cox3, rps, cox1, nad3, cox2). Phylogenetic analysis showed that the four mtDNAs were clustered with that of PM1 with high bootstrap support. Compared to mtDNA of PM1, the only non-synonymous mutation was located in nad2 (T505M) of strain PM26. Synonymous single nucleotide polymorphisms were observed at eight positions in the four mtDNAs.published_or_final_versio

Tsang, CC

Full Terms & Conditions of access and use can be found athttp://www.tandfonline.com/action/journalInformation?journalCode=tmdn20Mitochondrial DNA Part BResourcesISSN: (Print) 2380-2359 (Online) Journal homepage: http://www.tandfonline.com/loi/tmdn20Comparative mitogenomic and phylogeneticcharacterization on the complete mitogenomes ofTalaromyces (Penicillium) marneffeiEmily W. T. Tam, Chi-Ching Tsang, Susanna K. P. Lau & Patrick C. Y. WooTo cite this article: Emily W. T. Tam, Chi-Ching Tsang, Susanna K. P. Lau & Patrick C. Y.Woo (2016) Comparative mitogenomic and phylogenetic characterization on the completemitogenomes of Talaromyces (Penicillium) marneffei, Mitochondrial DNA Part B, 1:1, 941-942, DOI:10.1080/23802359.2016.1261610To link to this article:  https://doi.org/10.1080/23802359.2016.1261610© 2016 The Author(s). Published by InformaUK Limited, trading as Taylor & FrancisGroup.Published online: 04 Jan 2017.Submit your article to this journal Article views: 181View Crossmark dataCiting articles: 2 View citing articles MITOGENOME ANNOUNCEMENTComparative mitogenomic and phylogenetic characterization on the completemitogenomes of Talaromyces (Penicillium) marneffeiEmily W. T. Tama, Chi-Ching Tsanga , Susanna K. P. Laua,b,c,d,e and Patrick C. Y. Wooa,b,c,d,eaDepartment of Microbiology, The University of Hong Kong, Hong Kong; bState Key Laboratory of Emerging Infectious Diseases, TheUniversity of Hong Kong, Hong Kong; cResearch Centre of Infection and Immunology, The University of Hong Kong, Hong Kong; dCarol YuCentre of Infection, The University of Hong Kong, Hong Kong; eCollaborative Innovation Center for Diagnosis and Treatment of InfectiousDiseases, The University of Hong Kong, Hong KongABSTRACTWe report the complete mitochondrial DNA (mtDNA) sequences of four Talaromyces marneffei strainsand performed comparative genomic and phylogenetic analyses. The gene orders of the four mtDNAsare identical to the previously published mtDNA of strain PM1 (nad4l, nad5, nad2, atp9, cob, nad1,nad4, atp8, atp6, nad6, cox3, rps, cox1, nad3, cox2). Phylogenetic analysis showed that the four mtDNAswere clustered with that of PM1 with high bootstrap support. Compared to mtDNA of PM1, the onlynon-synonymous mutation was located in nad2 (T505M) of strain PM26. Synonymous single nucleotidepolymorphisms were observed at eight positions in the four mtDNAs.ARTICLE HISTORYReceived 4 November 2016Accepted 14 November 2016KEYWORDSMitogenome; Talaromycesmarneffei; Penicilliummarneffei; phylogeny;comparative genomicsTalaromyces (Penicillium) marneffei is the most important ther-mally dimorphic, systemic mycosis-causing fungus inSoutheast Asia (Vanittanakom et al. 2006). Apart from beingan AIDS-defining condition, penicilliosis has also beenreported in other immunocompromised patients (Chan et al.2016). Recently, we have described the emergence of penicil-liosis in patients on anti-CD20 monoclonal antibodies or kin-ase inhibitors (Chan et al. 2015). In 2003, we reported thecomplete mitochondrial DNA (mtDNA) sequence of T. marnef-fei strain PM1 (Woo et al. 2003). Subsequently, we havereported its draft genome sequence (Woo et al. 2011), sexualcycle-related genes (Woo et al. 2006), and polyketide syn-thase gene clusters (Woo et al. 2010). In this article, we reportthe complete mtDNA sequences of four additional T. marnef-fei strains (PM18, PM19, PM20, and PM26) and performedcomparative genomic and phylogenetic analyses. The fourstrains were isolated from penicilliosis patients in Hong Kong,and were deposited to the National Collection of PathogenicFungi (NCPF), UK (PM18¼NCPF 4320, PM19¼NCPF 4321,PM20¼NCPF 4322, and PM26¼NCPF 4323). Their mtDNAswere deposited in the International Nucleotide SequenceDatabases with accession numbers KU761329–KU761332.Talaromyces marneffei mtDNA was prepared from arthroco-nidia grown at 37 C and purified using the MitochondrialDNA Isolation Kit following manufacturer’s instructions(PromoKine, Heidelberg, Germany). The mtDNA was PCR-amplified using primers designed following the previouslypublished PM1–mtDNA sequence (Woo et al. 2003), and theamplified products were sequenced with an ABI PRISM 3130xlGenetic Analyzer (Applied Biosystems, Waltham, MA). Thesequences were assembled using CAP3 (Huang & Madan1999). Annotation was performed according to Woo et al.(2003). The four mtDNAs were aligned with the mtDNA ofPM1. Maximum-likelihood tree was reconstructed using MEGA7.0.14 (Kumar et al. 2016).The mtDNAs of the four T. marneffei strains are circularmolecules, with lengths of 35,420–35,436 bp and GþC con-tents of 24.6–25.1%. The gene orders of the four genomesare identical to that of PM1 (nad4l, nad5, nad2, atp9, cob,nad1, nad4, atp8, atp6, nad6, cox3, rps, cox1, nad3, cox2).63.6% of the four genomes are represented by structuralgenes (40.5% protein-coding exons, 5.9% tRNA genes, and17.3% rRNA genes), 8.8% by intergenic spacer, and 32.4% byintrons. They contain 15 genes encoding subunits of respira-tory chain complexes (cytochrome oxidase subunits I–III[cox1–cox3], apocytochrome b [cob], reduced nicotinamide-adenine dinucleotide-ubiquinone oxidoreductase subunits[nad1, nad2, nad3, nad4, nad4l, nad5, and nad6]), three ATPsynthase subunits (atp6, atp8, and atp9), and ribosomal pro-tein of the small ribosomal subunit (rps). Phylogenetic ana-lysis showed that the four mtDNAs were clustered with thatof PM1 with high bootstrap support (Figure 1). Compared toPM1 mtDNA, the only non-synonymous mutation was locatedin nad2 (T505M) of PM26. Synonymous single nucleotidepolymorphisms were observed in PM18 at T1088C, T506C,C9268T, T11060C, and C11845T located in nad5, cob, nad4,atp8, and atp6, respectively; in PM19 at C11845T located inatp6; in PM20 at G1674A located in nad2; and in PM26 atCONTACT Patrick C. Y. Woo pcywoo@hku.hk; Susanna K. P. Lau skplau@hku.hk Department of Microbiology, The University of Hong Kong, 4/F,University Pathology Building, Queen Mary Hospital, Hong Kong 2016 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use,distribution, and reproduction in any medium, provided the original work is properly cited.MITOCHONDRIAL DNA PART B: RESOURCES, 2016VOL. 1, NO. 1, 941–942http://dx.doi.org/10.1080/23802359.2016.1261610G29088A located in cox1. The four mtDNAs also encode 28tRNAs and the 23S and 16S rRNAs (rnl and rns).Disclosure statementThe authors report no conflicts of interest. The authors alone are respon-sible for the content and writing of the paper.FundingThis work was partly supported by the Health and Medical ResearchFund (Food and Health Bureau, the Government of the Hong KongSpecial Administrative Region, Hong Kong, under Grant HKM-15-M07[commissioned project]); the Strategic Research Theme Fund, TheUniversity of Hong Kong, Hong Kong; and the Croucher Senior MedicalResearch Fellowship, Croucher Foundation, Hong Kong.ORCIDChi-Ching Tsang http://orcid.org/0000-0001-6705-2866ReferencesChan JFW, Chan TSY, Gill H, Lam FYF, Trendell-Smith NJ, Sridhar S, Tse H,Lau SKP, Hung IFN, Yuen K-Y, et al. 2015. Disseminated infections withTalaromyces marneffei in non-AIDS patients given monoclonal antibod-ies against CD20 and kinase inhibitors. Emerg Infect Disease.21:1101–1106.Chan JFW, Lau SKP, Yuen K-Y, Woo PCY. 2016. Talaromyces (Penicillium)marneffei infection in non-HIV-infected patients. Emerg MicrobesInfect. 5:e19.Huang X, Madan A. 1999. CAP3: a DNA sequence assembly program.Genome Res. 9:868–877.Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular EvolutionaryGenetics Analysis Version 7.0 for bigger datasets. Mol Biol Evol.33:1870–1874.Vanittanakom N, Cooper CR, Fisher MC, Sirisanthana T. 2006. Penicilliummarneffei infection and recent advances in the epidemiology andmolecular biology aspects. Clin Microbiol Rev. 19:95–110.Woo PCY, Chong KTK, Tse H, Cai JJ, Lau CCY, Zhou AC, Lau SKP,Yuen K-Y. 2006. Genomic and experimental evidence for a potentialsexual cycle in the pathogenic thermal dimorphic fungus Penicilliummarneffei. FEBS Lett. 580:3409–3416.Woo PCY, Lau SKP, Liu B, Cai JJ, Chong KTK, Tse H, Kao RYT, Chan C-M,Chow W-N, Yuen K-Y. 2011. Draft genome sequence of Penicilliummarneffei strain PM1. Eukaryot Cell. 10:1740–1741.Woo PCY, Tam EWT, Chong KTK, Cai JJ, Tung ETK, Ngan AHY, Lau SKP,Yuen K-Y. 2010. High diversity of polyketide synthase genes and themelanin biosynthesis gene cluster in Penicillium marneffei. FEBS J.277:3750–3758.Woo PCY, Zhen H, Cai JJ, Yu J, Lau SKP, Wang J, Teng JLL, Wong SSY,Tse RH, Chen R, et al. 2003. The mitochondrial genome of the thermaldimorphic fungus Penicillium marneffei is more closely related to thoseof molds than yeasts. FEBS Lett. 555:469–477.Talaromycesmarneffei PM1 (AY347307)Talaromycesmarneffei PM26 (KU761331)Talaromycesmarneffei PM19 (KU761330)Talaromycesmarneffei PM20 (KU761331)Talaromycesmarneffei ATCC 18224T (JQ354997)Talaromycesmarneffei PM18 (KU761329)Talaromycesstipitatus ATCC 10500T(JQ354994)Aspergillus flavus TCM2014 (NC_026920)Aspergillus ustus 3.3904 (NC_025570)Aspergillus kawachii IFO 4308 (AP012272)Aspergillus niger N909 (NC_007445)Aspergillus tubingensis 0932 (NC_007597)Penicillium nordicum UASWS BFE487 (KR952336)Penicillium solitum 20-01 (NC_016187)Penicillium digitatum PHI26 (CM001645)Penicillium digitatum Pd1 (CM001644)Penicillium digitatum Pd01 (NC_015080)Penicillium roqueforti UASWS P1 (KR952335)10010010010010085721001001000.1Figure 1. Phylogenetic tree showing the relationship of Talaromyces marneffei strains PM18, PM19, PM20, and PM26 to other Aspergillus, Penicillium, andTalaromyces species. The tree was inferred from the concatenated mitochondrial gene (cox1, cox2, cox3, cob, nad1, nad2, nad3, nad4, nad4l, nad5, nad6, atp6, apt8,and atp9) sequence data by the maximum-likelihood method with the substitution model GTR (general time reversible model)þG (gamma-distributed rate vari-ation). The scale bar indicates the estimated number of substitutions per base. Numbers at nodes indicate levels of bootstrap support calculated from 1000 repli-cates. All names and accession numbers are given as cited in the International Nucleotide Sequence Databases.942 E. W. T. TAM ET AL.

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Comparative mitogenomic and phylogenetic characterization on the complete mitogenomes of Talaromyces (Penicillium) marneffei

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Comparative mitogenomic and phylogenetic characterization on the complete mitogenomes of <i>Talaromyces</i> (<i>Penicillium</i>) <i>marneffei</i>

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