[en] Lignin, a natural polyaromatic macromolecule, represents an essential component of the lignocellulose biomass. Due to its complexity, the natural degradation of this molecule by microorganisms still remains largely misunderstood. Extracellular oxidative degradation is followed by intracellular metabolic degradation of conserved aromatic intermediate compounds (protocatechuate, catechol, hydroxyquinol, and gentisic acid) that are used as carbon and energy sources. The lower funneling pathways are characterized by the opening of the aromatic ring of these molecules through dioxygenases, leading to degradation products that finally enter into the tricarboxylic acid (TCA) cycle. In order to better understand the adaptation mechanisms of Scedosporium species to their environment, these specific catabolism pathways were studied. Genes encoding ring-cleaving dioxygenases were identified in Scedosporium genomes by sequence homology, and a bioinformatic analysis of the organization of the corresponding gene clusters was performed. In addition, these predictions were confirmed by evaluation of the expression level of the genes of the gentisic acid cluster. When the fungus was cultivated in the presence of lignin or gentisic acid as sole carbon source, experiments revealed that the genes of the gentisic acid cluster were markedly overexpressed in the two Scedosporium species analyzed (Scedosporium apiospermum and Scedosporium aurantiacum). Only the gene encoding a membrane transporter was not overexpressed in the gentisic acid-containing medium. Together, these data suggest the involvement of the lower funneling pathways in Scedosporium adaptation to their environment.
Disciplines :
Microbiology
Author, co-author :
Poirier, Wilfried ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire ; UNIV Angers, UNIV Brest, Groupe d'Etude des Interactions Hôte-Pathogène (GEIHP), SFR ICAT, Angers, France
Ravenel, Kevin; UNIV Angers, UNIV Brest, Groupe d'Etude des Interactions Hôte-Pathogène (GEIHP), SFR ICAT, Angers, France
Bouchara, Jean-Philippe; UNIV Angers, UNIV Brest, Groupe d'Etude des Interactions Hôte-Pathogène (GEIHP), SFR ICAT, Angers, France
Giraud, Sandrine; UNIV Angers, UNIV Brest, Groupe d'Etude des Interactions Hôte-Pathogène (GEIHP), SFR ICAT, Angers, France
April T. M., Abbott S. P., Foght J. M., Currah R. S., (1998). Degradation of hydrocarbons in crude oil by the ascomycete Pseudallescheria boydii (Microascaceae). Can. J. Microbiol. 44, 270–278. doi: 10.1139/w97-152, PMID: 9606909
Azevedo E., Caeirao M. F., Rebelo R., Barata M., (2011). Biodiversity and characterization of marine mycota from Portuguese waters. Anim. Biodivers. Conserv. 34, 205–215.
Blasi B., Poyntner C., Rudavsky T., Prenafeta-Boldú F. X., Hoog S., de Tafer H., et al. (2016). Pathogenic yet environmentally friendly? Black fungal candidates for bioremediation of pollutants. Geomicrobiol J. 33, 308–317. doi: 10.1080/01490451.2015.1052118, PMID: 27019541
Bugg T. D., Ahmad M., Hardiman E. M., Singh R., (2011). The emerging role for bacteria in lignin degradation and bio-product formation. Curr. Opin. Biotechnol. 22, 394–400. doi: 10.1016/j.copbio.2010.10.009, PMID: 21071202
Buongiorno D., Straganz G. D., (2013). Structure and function of atypically coordinated enzymatic mononuclear non-heme-Fe(II) centers. Coord. Chem. Rev. 257, 541–563. doi: 10.1016/j.ccr.2012.04.028, PMID: 24850951
Cajthaml T., (2015). Biodegradation of endocrine-disrupting compounds by ligninolytic fungi: mechanisms involved in the degradation. Environ. Microbiol. 17, 4822–4834. doi: 10.1111/1462-2920.12460, PMID: 24650234
Cerqueira G. M., Kostoulias X., Khoo C., Aibinu I., Qu Y., Traven A., et al. (2014). A global virulence regulator in Acinetobacter baumannii and its control of the phenylacetic acid catabolic pathway. J. Infect. Dis. 210, 46–55. doi: 10.1093/infdis/jiu024, PMID: 24431277
Cimon B., Carrère J., Vinatier J. F., Chazalette J. P., Chabasse D., Bouchara J. P., (2000). Clinical significance of Scedosporium apiospermum in patients with cystic fibrosis. Eur. J. Clin. Microbiol. 19, 53–56. doi: 10.1007/s100960050011, PMID: 10706182
Claußen M., Schmidt S., (1998). Biodegradation of phenol and p-cresol by the hyphomycete Scedosporium apiospermum. Res. Microbiol. 149, 399–406. doi: 10.1016/S0923-2508(98)80322-7, PMID: 9766239
Claußen M., Schmidt S., (1999). Biodegradation of phenylbenzoate and some of its derivatives by Scedosporium apiospermum. Res. Microbiol. 150, 413–420. doi: 10.1016/s0923-2508(99)80077-1, PMID: 10466410
Cortez K. J., Roilides E., Quiroz-Telles F., Meletiadis J., Antachopoulos C., Knudsen T., et al. (2008). Infections caused by Scedosporium spp. Clin. Microbiol. Rev. 21, 157–197. doi: 10.1128/CMR.00039-07, PMID: 18202441
de Hoog G. S., Marvin-Sikkema F. D., Lahpoor G. A., Gottschall J. C., Prins R. A., Guého E., (1994). Ecology and physiology of the emerging opportunistic fungi Pseudallescheria boydii and Scedosporium prolificans. Mycoses 37, 71–78. doi: 10.1111/j.1439-0507.1994.tb00780.x, PMID: 7845423
Enguita F. J., Leitão A. L., (2013). Hydroquinone: environmental pollution, toxicity, and microbial answers. Biomed. Res. Int. 2013:542168. doi: 10.1155/2013/542168, PMID: 23936816
Eppinger E., Ferraroni M., Bürger S., Steimer L., Peng G., Briganti F., et al. (2015). Function of different amino acid residues in the reaction mechanism of gentisate 1, 2-dioxygenases deduced from the analysis of mutants of the salicylate 1, 2-dioxygenase from Pseudaminobacter salicylatoxidans. Biochim. Biophys. Acta 1854, 1425–1437. doi: 10.1016/j.bbapap.2015.06.005
Eppink M. H. M., Cammaart E., van Wassenaar D., Middelhoven W. J., van Berkel W. J. H., (2000). Purification and properties of hydroquinone hydroxylase, a FAD-dependent monooxygenase involved in the catabolism of 4-hydroxybenzoate in Candida parapsilosis CB604. Eur. J. Biochem. 267, 6832–6840. doi: 10.1046/j.1432-1033.2000.01783.x, PMID: 11082194
Gebhardt M. J., Gallagher L. A., Jacobson R. K., Usacheva E. A., Peterson L. R., Zurawski D. V., et al. (2015). Joint transcriptional control of virulence and resistance to antibiotic and environmental stress in Acinetobacter baumannii. mBio 6:e01660-15. doi: 10.1128/mBio.01660-15, PMID: 26556274
Gilgado F., Cano J., Gené J., Guarro J., (2005). Molecular phylogeny of the Pseudallescheria boydii species complex: proposal of two new species. J. Clin. Microbiol. 43, 4930–4942. doi: 10.1128/JCM.43.10.4930-4942.2005, PMID: 16207945
Gluck-Thaler E., Vijayakumar V., Slot J. C., (2018). Fungal adaptation to plant defenses through convergent assembly of metabolic modules. Mol. Ecol. 27, 5120–5136. doi: 10.1111/mec.14943, PMID: 30427102
Greene G. H., McGary K. L., Rokas A., Slot J. C., (2014). Ecology drives the distribution of specialized tyrosine metabolism modules in fungi. Genome Biol. Evol. 6, 121–132. doi: 10.1093/gbe/evt208, PMID: 24391152
Guarro J., Kantarcioglu A. S., Horré R., Rodriguez-Tudela J. L., Cuenca Estrella M., Berenguer J., et al. (2006). Scedosporium apiospermum: changing clinical spectrum of a therapy-refractory opportunist. Med. Mycol. 44, 295–327. doi: 10.1080/13693780600752507, PMID: 16772225
Harun A., Gilgado F., Chen S. C., Meyer W., (2010). Abundance of Pseudallescheria/Scedosporium species in the Australian urban environment suggests a possible source for scedosporiosis including the colonization of airways in cystic fibrosis. Med. Mycol. 48(Suppl. 1), S70–S76. doi: 10.3109/13693786.2010.515254
Harwood C. S., Parales R. E., (1996). The β-ketoadipate pathway and the biology of self-identity. Annu. Rev. Microbiol. 50, 553–590. doi: 10.1146/annurev.micro.50.1.553, PMID: 8905091
Johnson C. W., Beckham G. T., (2015). Aromatic catabolic pathway selection for optimal production of pyruvate and lactate from lignin. Metab. Eng. 28, 240–247. doi: 10.1016/j.ymben.2015.01.005, PMID: 25617773
Jones D. T., Taylor W. R., Thornton J. M., (1992). The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8, 275–282. doi: 10.1093/bioinformatics/8.3.275
Kaltseis J., Rainer J., De Hoog G. S., (2009). Ecology of Pseudallescheria and Scedosporium species in human-dominated and natural environments and their distribution in clinical samples. Med. Mycol. 47, 398–405. doi: 10.1080/13693780802585317, PMID: 19085459
Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., et al. (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649. doi: 10.1093/bioinformatics/bts199, PMID: 22543367
Kirk P. W., (1967). A comparison of saline tolerance and sporulation in marine and clinical isolates of Allescheria boydii shear. Mycopathol. Mycol. Appl. 33, 65–75. doi: 10.1007/BF02049792
Korniłłowicz-Kowalska T., Rybczyńska K., (2015). Screening of microscopic fungi and their enzyme activities for decolorization and biotransformation of some aromatic compounds. Int. J. Environ. Sci. Technol. 12, 2673–2686. doi: 10.1007/s13762-014-0656-2
Kumar S., Stecher G., Li M., Knyaz C., Tamura K., (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549. doi: 10.1093/molbev/msy096, PMID: 29722887
Lasota S., Stephan I., Horn M. A., Otto W., Noll M., (2018). Copper in wood preservatives delayed wood decomposition and shifted soil fungal but not bacterial community composition. Appl. Environ. Microbiol. 85:e02391-18. doi: 10.1128/AEM.02391-18, PMID: 30530712
Liu C., Zheng H., Yang M., Xu Z., Wang X., Wei L., et al. (2015). Genome analysis and in vivo virulence of porcine extraintestinal pathogenic Escherichia coli strain PCN033. BMC Genomics 16:717. doi: 10.1186/s12864-015-1890-9, PMID: 26391348
Livak K. J., Schmittgen T. D., (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408. doi: 10.1006/meth.2001.1262, PMID: 11846609
Lubbers R. J. M., Dilokpimol A., Visser J., Mäkelä M. R., Hildén K. S., de Vries R. P., (2019). A comparison between the homocyclic aromatic metabolic pathways from plant-derived compounds by bacteria and fungi. Biotechnol. Adv. 37:107396. doi: 10.1016/j.biotechadv.2019.05.002, PMID: 31075306
Ma X., Zhang B., Liu B., (2020). Analysis of fungal diversity of the rotten wooden pillars of a historic building. Res. Square [Preprint]. doi: 10.21203/rs.2.23473/v1
Mäkelä M. R., Marinović M., Nousiainen P., Liwanag A. J. M., Benoit I., Sipilä J., et al. (2015). Aromatic metabolism of filamentous fungi in relation to the presence of aromatic compounds in plant biomass. Adv. Appl. Microbiol. 91, 63–137. doi: 10.1016/bs.aambs.2014.12.001
Marchler-Bauer A., Derbyshire M. K., Gonzales N. R., Lu S., Chitsaz F., Geer L. Y., et al. (2015). CDD: NCBI’s conserved domain database. Nucleic Acids Res. 43, D222–D226. doi: 10.1093/nar/gku1221, PMID: 25414356
Martins T. M., Hartmann D. O., Planchon S., Martins I., Renaut J., Silva Pereira C., (2015). The old 3-oxoadipate pathway revisited: new insights in the catabolism of aromatics in the saprophytic fungus Aspergillus nidulans. Fungal Genet. Biol. 74, 32–44. doi: 10.1016/j.fgb.2014.11.002, PMID: 25479309
Martins T. M., Martins C., Silva Pereira C., (2019). Multiple degrees of separation in the central pathways of the catabolism of aromatic compounds in fungi belonging to the Dikarya sub-kingdom. Adv. Microb. Physiol. 75, 177–203. doi: 10.1016/bs.ampbs.2019.07.003
Martins C., Varela A., Leclercq C. C., Núñez O., Větrovský T., Renaut J., et al. (2018). Specialisation events of fungal metacommunities exposed to a persistent organic pollutant are suggestive of augmented pathogenic potential. Microbiome 6:208. doi: 10.1186/s40168-018-0589-y, PMID: 30466483
Michielse C. B., Reijnen L., Olivain C., Alabouvette C., Rep M., (2012). Degradation of aromatic compounds through the β-ketoadipate pathway is required for pathogenicity of the tomato wilt pathogen Fusarium oxysporum f. sp. lycopersici: β-Ketoadipate pathway is required for pathogenicity. Mol. Plant Pathol. 13, 1089–1100. doi: 10.1111/j.1364-3703.2012.00818.x, PMID: 22827542
Naoumkina M. A., Zhao Q., Gallego-Giraldo L., Dai X., Zhao P. X., Dixon R. A., (2010). Genome-wide analysis of phenylpropanoid defence pathways. Mol. Plant Pathol. 11, 829–846. doi: 10.1111/j.1364-3703.2010.00648.x, PMID: 21029326
Nirma C., Eparvier V., Stien D., (2013). Antifungal agents from Pseudallescheria boydii SNB-CN73 isolated from a Nasutitermes sp. termite. J. Nat. Prod. 76, 988–991. doi: 10.1021/np4001703, PMID: 23627396
Penn C. D., Daniel S. L., (2013). Salicylate degradation by the fungal plant pathogen Sclerotinia sclerotiorum. Curr. Microbiol. 67, 218–225. doi: 10.1007/s00284-013-0349-y, PMID: 23512122
Perez-Cuesta U., Aparicio-Fernandez L., Guruceaga X., Martin-Souto L., Abad-Diaz-de-Cerio A., Antoran A., et al. (2020). Melanin and pyomelanin in Aspergillus fumigatus: from its genetics to host interaction. Int. Microbiol. 23, 55–63. doi: 10.1007/s10123-019-00078-0, PMID: 31020477
Pérez-Pantoja D., De la Iglesia R., Pieper D. H., González B., (2008). Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutant-degrading bacterium Cupriavidus necator JMP134. FEMS Microbiol. Rev. 32, 736–794. doi: 10.1111/j.1574-6976.2008.00122.x, PMID: 18691224
Pfaffl M. W., (2001). A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29:e45. doi: 10.1093/nar/29.9.e45, PMID: 11328886
Pham T., Giraud S., Schuliar G., Rougeron A., Bouchara J.-P., (2015). Scedo-select III: a new semi-selective culture medium for detection of the Scedosporium apiospermum species complex. Med. Mycol. 53, 512–519. doi: 10.1093/mmy/myv015, PMID: 25841055
Pihet M., Carrere J., Cimon B., Chabasse D., Delhaes L., Symoens F., et al. (2009). Occurrence and relevance of filamentous fungi in respiratory secretions of patients with cystic fibrosis – a review. Med. Mycol. 47, 387–397. doi: 10.1080/13693780802609604, PMID: 19107638
Prenafeta-Boldú F. X., Summerbell R., Sybren de Hoog G., (2006). Fungi growing on aromatic hydrocarbons: biotechnology’s unexpected encounter with biohazard? FEMS Microbiol. Revue 30, 109–130. doi: 10.1111/j.1574-6976.2005.00007.x, PMID: 16438682
Rojas-Jiménez K., Hernández M., (2015). Isolation of fungi and bacteria associated with the guts of tropical wood-feeding coleoptera and determination of their lignocellulolytic activities. Int. J. Microbiol. 2015:285018. doi: 10.1155/2015/285018, PMID: 26379709
Rougeron A., Giraud S., Alastruey-Izquierdo A., Cano-Lira J., Rainer J., et al. (2018). Ecology of Scedosporium species: present knowledge and future research. Mycopathologia 183, 185–200. doi: 10.1007/s11046-017-0200-2, PMID: 28929280
Rougeron A., Schuliar G., Leto J., Sitterlé E., Landry D., Bougnoux M.-E., et al. (2015). Human-impacted areas of France are environmental reservoirs of the Pseudallescheria boydii/Scedosporium apiospermum species complex. Environ. Microbiol. 17, 1039–1048. doi: 10.1111/1462-2920.12472, PMID: 24684308
Sbaghi M., Jeandet P., Bessis R., Leroux P., (1996). Degradation of stilbene-type phytoalexins in relation to the pathogenicity of Botrytis cinerea to grapevines. Plant Pathol. 45, 139–144. doi: 10.1046/j.1365-3059.1996.d01-101.x
Semana P., Powlowski J., (2019). Four aromatic intradiol ring cleavage dioxygenases from Aspergillus niger. Appl. Environ. Microbiol. 85:e01786-19. doi: 10.1128/AEM.01786-19, PMID: 31540981
Sillitoe I., Bordin N., Dawson N., Waman V. P., Ashford P., Scholes H. M., et al. (2021). CATH: increased structural coverage of functional space. Nucleic Acids Res. 49, D266–D273. doi: 10.1093/nar/gkaa1079, PMID: 33237325
Tigini V., Prigione V., Varese G. C., (2014). Mycological and ecotoxicological characterisation of landfill leachate before and after traditional treatments. Sci. Total Environ. 487, 335–341. doi: 10.1016/j.scitotenv.2014.04.026
Vandeputte P., Ghamrawi S., Rechenmann M., Iltis A., Giraud S., Fleury M., et al. (2014). Draft genome sequence of the pathogenic fungus Scedosporium apiospermum. Genome Announc. 2:e00988-14. doi: 10.1128/genomeA.00988-14, PMID: 25278533
Wang H., Chen H., Hao G., Yang B., Feng Y., Wang Y., et al. (2013). Role of the phenylalanine-hydroxylating system in aromatic substance degradation and lipid metabolism in the oleaginous fungus Mortierella alpina. Appl. Environ. Microbiol. 79, 3225–3233. doi: 10.1128/AEM.00238-13, PMID: 23503309
Wang W., Zhang C., Sun X., Su S., Li Q., Linhardt R. J., (2017). Efficient, environmentally-friendly and specific valorization of lignin: promising role of non-radical lignolytic enzymes. World J. Microbiol. Biotechnol. 33:125. doi: 10.1007/s11274-017-2286-6, PMID: 28752265
Westphal A. H., Tischler D., van Berkel W. J. H., (2021). Natural diversity of FAD-dependent 4-hydroxybenzoate hydroxylases. Arch. Biochem. Biophys. 702:108820. doi: 10.1016/j.abb.2021.108820, PMID: 33684360
Wu Q., Jiang N., Bo Han W., Ning Mei Y., Ming Ge H., Kai Guo Z., et al. (2014). Antibacterial epipolythiodioxopiperazine and unprecedented sesquiterpene from Pseudallescheria boydii, a beetle (coleoptera)-associated fungus. Org. Biomol. Chem. 12, 9405–9412. doi: 10.1039/C4OB01494D, PMID: 25319640
