Transcriptional Interplay between Malassezia restricta and Staphylococcus Species Co-Existing in the Skin Environment
2
조회
0
다운로드
0
인용
0
참고문헌
키워드
초록
Malassezia and Staphylococcus are the most dominant genera in human skin microbiome. To explore the inter-kingdom interactions between the two genera, we examined the transcriptional changes in Malassezia and Staphylococcus species induced upon co-culturing. RNA-seq analyses revealed that genes encoding ribosomal proteins were upregulated, while those encoding aspartyl proteases were downregulated in M. restricta after co-culturing with Staphylococcus species. We identified MRET_3770 as a major secretory aspartyl protease coding gene in M. restricta through pepstatin-A affinity chromatography followed by mass spectrometry and found that the expression of MRET_3770 was significantly repressed upon co-culturing with Staphylococcus species or by incubation in media with reduced pH. Moreover, biofilm formation by Staphylococcus aureus was inhibited in the spent medium of M. restricta, suggesting that biomolecules secreted by M. restricta such as secretory aspartyl proteases may degrade the biofilm structure. We also examined the transcriptional changes in S. aureus co-cultured with M. restricta and found co-cultured S. aureus showed increased expression of genes encoding ribosomal proteins and downregulation of those involved in riboflavin metabolism. These transcriptome data of co-cultured fungal and bacterial species demonstrate a dynamic interplay between the two co-existing genera.
Abstract
Malassezia and Staphylococcus are the most dominant genera in human skin microbiome. To explore the inter-kingdom interactions between the two genera, we examined the transcriptional changes in Malassezia and Staphylococcus species induced upon co-culturing. RNA-seq analyses revealed that genes encoding ribosomal proteins were upregulated, while those encoding aspartyl proteases were downregulated in M. restricta after co-culturing with Staphylococcus species. We identified MRET_3770 as a major secretory aspartyl protease coding gene in M. restricta through pepstatin-A affinity chromatography followed by mass spectrometry and found that the expression of MRET_3770 was significantly repressed upon co-culturing with Staphylococcus species or by incubation in media with reduced pH. Moreover, biofilm formation by Staphylococcus aureus was inhibited in the spent medium of M. restricta, suggesting that biomolecules secreted by M. restricta such as secretory aspartyl proteases may degrade the biofilm structure. We also examined the transcriptional changes in S. aureus co-cultured with M. restricta and found co-cultured S. aureus showed increased expression of genes encoding ribosomal proteins and downregulation of those involved in riboflavin metabolism. These transcriptome data of co-cultured fungal and bacterial species demonstrate a dynamic interplay between the two co-existing genera.
참고문헌 (40)
- Schlecht LM, "Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue", Microbiology, 161, pp.168~181 (2015)
- Bumroongthai K, "Biofilm production and antifungal susceptibility of co-cultured Malassezia pachydermatis and Candida parapsilosis isolated from canine seborrheic dermatitis", Med. Mycol, 54, pp.544~549 (2016)
- Janus MM, "Candida albicans in multispecies oral communities; a keystone commensal?", Adv. Exp. Med. Biol, 931, pp.13~20 (2016)
- Lee K, "Co-infection of Malassezia sympodialis with bacterial pathobionts Pseudomonas aeruginosa or Staphylococcus aureus leads to distinct sinonasal inflammatory responses in a murine acute sinusitis model", Front. Cell Infect. Microbiol, 10, pp.472~ (2020)
- Warmink JA, "Migratory response of soil bacteria to Lyophyllum sp. strain Karsten in soil microcosms", Appl. Environ. Microbiol, 75, pp.2820~2830 (2009)
- Schroeckh V, "Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans", Proc. Natl. Acad. Sci. USA, 106, pp.14558~14563 (2009)
- Kastman EK, "Biotic Interactions shape the ecological distributions of Staphylococcus species", mBio, 7, pp.e01157-16~ (2016)
- Chen Y, "Wheat microbiome bacteria can reduce virulence of a plant pathogenic fungus by altering histone acetylation", Nat. Commun, 9, pp.3429~ (2018)
- Schmid-Wendtner MH, "The pH of the skin surface and its impact on the barrier function", Skin Pharmacol. Physiol, 19, pp.296~302 (2006)
- Grice EA, "The skin microbiome", Nat. Rev. Microbiol, 9, pp.244~253 (2011)
- Boxberger M, "Challenges in exploring and manipulating the human skin microbiome", Microbiome, 9, pp.125~ (2021)
- Riesenfeld CS, "Metagenomics: genomic analysis of microbial communities", Annu. Rev. Genet, 38, pp.525~552 (2004)
- Byrd AL, "The human skin microbiome", Nat. Rev. Microbiol, 16, pp.143~155 (2018)
- Belkaid Y, "Dialogue between skin microbiota and immunity", Science, 346, pp.954~959 (2014)
- Findley K, "Topographic diversity of fungal and bacterial communities in human skin", Nature, 498, pp.367~370 (2013)
- 박민지, "Skin Commensal Fungus Malassezia and Its Lipases", Journal of Microbiology and Biotechnology, 31(5), pp.637~644 (2021), 한국미생물·생명공학회[DOI]
- Chua W, "Secretory proteases of the human skin microbiome", Infect. Immun, 90, pp.e0039721~ (2022)
- Poh SE, "Identification of Malassezia furfur secreted aspartyl protease 1(MfSAP1) and its role in extracellular matrix degradation", Front. Cell Infect. Microbiol, 10, pp.148~ (2020)
- Li H, "Skin commensal Malassezia globosa secreted protease attenuates Staphylococcus aureus biofilm formation", J. Invest. Dermatol, 138, pp.1137~1145 (2018)
- Martin DE, "TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1", Cell, 119, pp.969~979 (2004)
- Warner JR, "The economics of ribosome biosynthesis in yeast", Trends Biochem. Sci, 24, pp.437~440 (1999)
- Nomura M, "Ribosomal RNA genes, RNA polymerases, nucleolar structures, and synthesis of rRNA in the yeast Saccharomyces cerevisiae", Cold Spring Harb Symp. Quant. Biol, 66, pp.555~565 (2001)
- Lund PA, "Understanding how microorganisms respond to acid pH Is central to their control and successful exploitation", Front. Microbiol, 11, pp.556140~ (2020)
- Goh JPZ, "The human pathobiont Malassezia furfur secreted protease Mfsap1 regulates cell dispersal and exacerbates skin inflammation", Proc. Natl. Acad. Sci. USA, 119, pp.e2212533119~ (2022)
- Nomura M, "Regulation of the synthesis of ribosomes and ribosomal components", Annu. Rev. Biochem, 53, pp.75~117 (1984)
- Lemke JJ, "Direct regulation of Escherichia coli ribosomal protein promoters by the transcription factors ppGpp and DksA", Proc. Natl. Acad. Sci. USA, 108, pp.5712~5717 (2011)
- Wang H, "Dual-targeting small-molecule inhibitors of the Staphylococcus aureus FMN riboswitch disrupt riboflavin homeostasis in an infectious setting", Cell Chem. Biol, 24, pp.576~588 e576 (2017)
- Gutierrez-Preciado A, "Extensive identification of bacterial riboflavin transporters and their distribution across bacterial species", PLoS One, 10, pp.e0126124~ (2015)
- Vitreschak AG, "Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation", Nucleic Acids Res, 30, pp.3141~3151 (2002)
- Serganov A, "Coenzyme recognition and gene regulation by a flavin mononucleotide riboswitch", Nature, 458, pp.233~237 (2009)
- Gelfand MS, "A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes", Trends Genet, 15, pp.439~442 (1999)
- Fischer M, "Biosynthesis of flavocoenzymes", Nat. Prod. Rep, 22, pp.324~350 (2005)
- Zhang P, "Structure and mechanism of the S component of a bacterial ECF transporter", Nature, 468, pp.717~720 (2010)
- Midgley G, "The diversity of Pityrosporum (Malassezia) yeasts in vivo and in vitro", Mycopathologia, 106, pp.143~153 (1989)
- Leeming JP, "Improved methods for isolation and enumeration of Malassezia furfur from human skin", J. Clin. Microbiol, 25, pp.2017~2019 (1987)
- Doyle JE, "Limitations of thioglycolate broth as a sterility test medium for materials exposed to gaseous ethylene oxide", Appl. Microbiol, 16, pp.1742~1744 (1968)
- Bolger AM, "Trimmomatic: a flexible trimmer for illumina sequence data", Bioinformatics, 30, pp.2114~2120 (2014)
- Kim D, "Graph-based genome alignment and genotyping with HISAT2 and HISATgenotype", Nat. Biotechnol, 37, pp.907~915 (2019)
- Liao Y, "The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote", Nucleic Acids Res, 41, pp.e108~ (2013)
- Love MI, "Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2", Genome Biol, 15, pp.550~ (2014)
