Draft genome of Gongronella butleri reveals the genes contributing to its biodegradation potential
Tóm tắt
Gongronella butleri is a fungus with many industrial applications including the composting of solid biowaste. Kerala Agricultural University, India, has developed a microbial consortium of which GbKAU strain of G. butleri is a major component. Even with great industrial significance, genome of this fungus is not published, and the genes and pathways contributing to the applications are not understood. This study had the objective to demonstrate the solid biowaste decomposing capability of the strain, to sequence and annotate the genome, and to reveal the genes and pathways contributing to its biodegradation potential. Strain GbKAU of G. butleri isolated and purified from the organic compost was found to produce higher levels of laccase and amylase, compared to Bacillus subtilis which is being widely used in biosolid waste management. Both were shown to be equally efficient in the in vivo composting capabilities. Whole genome sequencing has given ~11 million paired-end good quality reads. De novo assembly using dual-fold approach has yielded 44,639 scaffolds with draft genome size of 29.8 Mb. A total of 11,428 genes were predicted and classified into 359 groups involved in diverse pathways, of which 14 belonged to the enzymes involved in the degradation of macromolecules. Seven previously sequenced strains of the fungus were assembled and annotated. A direct comparison showed that the number of genes present in those strains was comparable to our strain, while all the important biodegrading genes were conserved across the genomes. Gene Ontology analysis had classified the genes according to their molecular function, biological process, and cellular component. A total of 104,718 SSRs were mined and classified to mono- to hexa-nucleotide repeats. The variant analysis in comparison with the closely related genus Cunninghamella has revealed 1156 variants. Apart from demonstrating the biodegradation capabilities of the GbKAU strain of G. butleri, the genome of this industrially important fungus was sequenced, de novo assembled, and annotated. GO analysis has classified the genes based on their functions, and the genes involved in biodegradation were revealed. Biodegradation potential, genome features in comparison with other strains, and the functions of the identified genes are discussed.
Tài liệu tham khảo
Awasthi MK, Pandey AK, Khan J, Bundela PS, Wong JW, Selvam A (2014) Evaluation of thermophilic fungal consortium for organic municipal solid waste composting. Bioresour Technol 168:214–221. https://doi.org/10.1016/j.biortech.2014.01.048
Awasthi MK, Pandey AK, Bundela PS, Khan J (2015) Co-composting of organic fraction of municipal solid waste mixed with different bulking waste: characterization of physicochemical parameters and microbial enzymatic dynamic. Bioresour Technol 182:200–207. https://doi.org/10.1016/j.biortech.2015.01.104
Awasthi MK, Wang Q, Ren X, Zhao J, Huang H, Awasthi SK, Lahori AH, Li R, Zhou L, Zhang Z (2016) Role of biochar amendment in mitigation of nitrogen loss and greenhouse gas emission during sewage sludge composting. Bioresour Technol 219:270–280. https://doi.org/10.1016/j.biortech.2016.07.128
Voběrková S, Vaverková MD, Burešová A, Adamcová D, Vršanská M, Kynický J, Brtnický M, Adam V (2017) Effect of inoculation with white-rot fungi and fungal consortium on the composting efficiency of municipal solid waste. Waste Manag 61:157–164. https://doi.org/10.1016/j.wasman.2016.12.039
Ke GR, Lai CM, Liu YY, Yang SS (2010) Inoculation of food waste with the thermo-tolerant lipolytic actinomycete Thermoactinomyces vulgaris A31 and maturity evaluation of the compost. Bioresour Technol 101(19):7424–7431. https://doi.org/10.1016/j.biortech.2010.04.051
Nakasaki K, Araya S, Mimoto H (2013) Inoculation of Pichia kudriavzevii RB1 degrades the organic acids present in raw compost material and accelerates composting. Bioresour Technol 144:521–528. https://doi.org/10.1016/j.biortech.2013.07.005
Bartnicki-Garcia S (1968) Cell wall chemistry, morphogenesis, and taxonomy of fungi. Annu Rev Microbiol 22(1):87–108. https://doi.org/10.1146/annurev.mi.22.100168.000511
Nwe N, Furuike T, Tamura H (2009) The mechanical and biological properties of chitosan scaffolds for tissue regeneration templates are significantly enhanced by chitosan from Gongronella butleri. Materials 2(2):374–398. https://doi.org/10.3390/ma2020374
Hirano S, Tobetto K, Hasegawa M, Matsuda N (1980) Permeability properties of gels and membranes derived from chitosan. J Biomed Mater Res 14(4):477–485. https://doi.org/10.1002/jbm.820140414
Pospieszny H, Chirkov S, Atabekov J (1991) Induction of antiviral resistance in plants by chitosan. Plant Sci 79(1):63–68. https://doi.org/10.1016/0168-9452(91)90070-O
Ikeda I, Sugano M, Yoshida K, Sasaki E, Iwamoto Y, Hatano K (1993) Effects of chitosan hydrolyzates on lipid absorption and on serum and liver lipid concentration in rats. J Agric Food Chem 41(3):431–435. https://doi.org/10.1021/jf00027a016
Nge KL, Nwe N, Chandrkrachang S, Stevens WF (2006) Chitosan as a growth stimulator in orchid tissue culture. Plant Sci 170(6):1185–1190. https://doi.org/10.1016/j.plantsci.2006.02.006
Shilpa P (2019) Microbial inoculants for enhancing degradation of biosolid waste in aerobic composting. M. Sc. Thesis, Kerala Agricultural University, India.
Valsalan R, Mathew D (2020) Draft genome of Meyerozyma guilliermondii strain vka1, a yeast strain with composting potential. J Genet Eng Biotechnol 18:54. https://doi.org/10.1186/s43141-020-00074-2
Kollerov VV, Shutov AA, Fokina VV, Sukhodol'skaya GV, Donova MV (2008) Biotransformation of 3-keto-androstanes by Gongronella butleri VKM F-1033. J Mol Catal B Enzym 55(1-2):61–68. https://doi.org/10.1016/j.molcatb.2008.01.009
Santos FRS, Garcia NFL, da Paz MF, Fonseca GG, Leite RSR (2016) Production and characterization of β-glucosidase from Gongronella butleri by solid-state fermentation. Afr J Biotechnol 15(16):633–641. https://doi.org/10.5897/AJB2015.15025
Carballeira J, Valmaseda M, Alvarez E, Gago JS (2004) Gongronella butleri, Schizosaccharomyces octosporus and Diplogelasinospora grovesii: novel microorganisms useful for the stereoselective reduction of ketones. Enzym Microb Technol 34(6):611–623. https://doi.org/10.1016/j.enzmictec.2004.02.002
Cavalheiro GF, Sanguine IS, Santos FRS, Costa AC, Fernandes M, Paz MF, Fonseca GG, Leite RS (2017) Catalytic properties of amylolytic enzymes produced by Gongronella butleri using agroindustrial residues on solid-state fermentation. Biomed Res Int 2017:7507523. https://doi.org/10.1155/2017/7507523
Akone SH, Rahn S, Henrich B, Daletos G, Vardamides JC, Nkengfack AE, Lin W, Lai D, Proksch P (2014) 2-Pentenedioic acid derivatives from a soil-derived fungus Gongronella butleri. Phytochem Lett 10:184–188. https://doi.org/10.1016/j.phytol.2014.09.001
Gnanesh BN, Tejaswi A, Arunakumar GS, Supriya M, Manojkumar HB, Tewary P (2021) Molecular phylogeny, identification and pathogenicity of Rhizopus oryzae associated with root rot of mulberry in India. J Appl Microbiol 131(1):360–374. https://doi.org/10.1111/jam.14959
Liu K, Ding X, Deng B, Chen W (2009) Isolation and characterization of endophytic taxol-producing fungi from Taxus chinensis. J Ind Microbiol Biotechnol 36(9):1171. https://doi.org/10.1007/s10295-009-0598-8
Siu-Rodas Y, de los Angeles Calixto-Romo M, Guillén-Navarro K, Sánchez JE, Zamora-Briseno JA, Amaya-Delgado L (2018) Bacillus subtilis with endocellulase and exocellulase activities isolated in the thermophilic phase from composting with coffee residues. Rev Argent Microbiol 50(3):234–243. https://doi.org/10.1016/j.ram.2017.08.005
Grgić DK, Domanovac MV, Domanovac T, Šabić M, Cvetnić M, Bulatović VO (2019) Influence of Bacillus subtilis and Pseudomonas aeruginosa BSW and clinoptilolite addition on the biowaste composting process. Arab J Sci Eng 44(6):5399–5409. https://doi.org/10.1007/s13369-018-03692-8
Sadasivam S, Manickam A (2008) Biochemical methods, 3rd edn. New Age International, New Delhi, p 284 ISBN 9788122421408
Telke AA, Kalyani DC, Jadhav UU, Parshetti GK, Govindwar SP (2009) Purification and characterization of an extracellular laccase from a pseudomonas sp. LBC1 and its application for the removal of bisphenol a. J Mol Catal B Enzym 61(3-4):252–260. https://doi.org/10.1016/j.molcatb.2009.08.001
Shilpa P, Girija D (2021) Microbial consortium for efficient composting of biosolid waste. J Trop Agric 59(1):71–75
Duan M, Zhang Y, Zhou B, Qin Z, Wu J, Wang Q, Yin Y (2020) Effects of Bacillus subtilis on carbon components and microbial functional metabolism during cow manure-straw composting. Bioresour Technol 303:122868. https://doi.org/10.1016/j.biortech.2020.122868
Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Report 1:19–21. https://doi.org/10.1007/BF02712670
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data Babraham Bioinformatics, Babraham Institute, Cambridge, United Kingdom Available at http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ retrieved 19 Aug 2021
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021
Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19(6):1117–1123. https://doi.org/10.1101/gr.089532.108
Stanke M, Diekhans M, Baertsch R, Haussler D (2008) Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24(5):637–644. https://doi.org/10.1093/bioinformatics/btn013
Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35(Suppl_2):W182–W185. https://doi.org/10.1093/nar/gkm321
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinf 10:421. https://doi.org/10.1186/1471-2105-10-421
Hesseltine CW, Ellis JJ (1964) The genus Ahsidia: Gongronella and cylindrical-spored species of Absidio. Mycologia 56(4):568–601. https://doi.org/10.1080/00275514.1964.12018145
Babu AG, Kim SW, Adhikari M, Yadav DR, Um YH, Kim C, Lee HB, Lee YS (2015) A new record of Gongronella butleri isolated in Korea. Mycobiology 43(2):166–169. https://doi.org/10.5941/MYCO.2015.43.2.166
Yin LJ, Lin HH, Xiao ZR (2010) Purification and characterization of a cellulase from Bacillus subtilis YJ1. J Mar Sci Technol 18(3):466–471
Koenig A, Bari QH (2000) Application of self-heating test for indirect estimation of respirometric activity of compost: theory and practice. Compost Sci Util 8(2):99–107. https://doi.org/10.1080/1065657X.2000.10701755
Kircher M, Heyn P, Kelso J (2011) Addressing challenges in the production and analysis of Illumina sequencing data. BMC Genomics 12:382. https://doi.org/10.1186/1471-2164-12-382
Lin Y, Li J, Shen H, Zhang L, Papasian CJ, Deng HW (2011) Comparative studies of de novo assembly tools for next-generation sequencing technologies. Bioinformatics 27(15):2031–2037. https://doi.org/10.1093/bioinformatics/btr319
Aoki-Kinoshita KF, Kanehisa M (2007) Gene annotation and pathway mapping in KEGG. In: Bergman NH (ed) Comparative genomics Vol 2, methods in molecular biology™, vol 396. Humana Press, pp 71–91. https://doi.org/10.1007/978-1-59745-515-2_6
Kanamori T, Kanou N, Atomi H, Imanaka T (2004) Enzymatic characterization of a prokaryotic urea carboxylase. J Bacteriol 186(9):2532–2539. https://doi.org/10.1128/JB.186.9.2532-2539.2004
Ohta T, Tani A, Kimbara K, Kawai F (2005) A novel nicotinoprotein aldehyde dehydrogenase involved in polyethylene glycol degradation. Appl Microbiol Biotechnol 68(5):639–646. https://doi.org/10.1007/s00253-005-1936-z
Li X, Li Y, Wei D, Li P, Wang L, Feng L (2010) Characterization of a broad-range aldehyde dehydrogenase involved in alkane degradation in Geobacillus thermodenitrificans NG80-2. Microbiol Res 165(8):706. https://doi.org/10.1016/j.micres.2010.01.006
Kawai F (2002) Microbial degradation of polyethers. Appl Microbiol Biotechnol 58:30–38. https://doi.org/10.1007/s00253-001-0850-2
Koenig K, Andreesen JR (1989) Molybdenum involvement in aerobic degradation of 2-furoic acid by pseudomonas putida Fu1. Appl Environ Microbiol 55(7):18291–11834. https://doi.org/10.1128/aem.55.7.1829-1834.1989
Modig T, Lidén G, Taherzadeh MJ (2002) Inhibition effects of furfural on alcohol dehydrogenase, aldehyde dehydrogenase and pyruvate dehydrogenase. Biochem J 363(3):769–776. https://doi.org/10.1042/bj3630769
Koopman F, Wierckx N, DeWinde JH, Ruijssenaars HJ (2010) Identification and characterization of the furfural and 5-(hydroxymethyl)furfural degradation pathways of Cupriavidus basilensis HMF 14. Proc Natl Acad Sci U S A 107(11):4919–4924. https://doi.org/10.1073/pnas.0913039107
Gaziola S, Sodek L, Arruda P, Lea P, Azevedo R (2000) Degradation of lysine in rice seeds: effect of calcium, ionic strength, S-adenosylmethionine and S-2-aminoethyl-l-cysteine on the lysine 2-oxoglutarate reductase-saccharopine dehydrogenase bifunctional enzyme. Physiol Plant 110(2):164–171. https://doi.org/10.1034/j.1399-3054.2000.110204.x
Pompeu GB, Vendemiatti A, Gratão PL, Gaziola SA, Lea PJ, Azevedo RA (2006) Saccharopine dehydrogenase activity in the high-lysine opaque and floury maize mutants. Food Biotechnol 20(1):55–64. https://doi.org/10.1080/08905430500524101
de Mello Serrano GC, Kiyota E, Zanata N, Arruda P (2012) Lysine degradation through the saccharopine pathway in bacteria: LKR and SDH in bacteria and its relationship to the plant and animal enzymes. FEBS Lett 586(6):905–911. https://doi.org/10.1016/j.febslet.2012.02.023
Oppermann FB, Schmidt B, Steinbüchel A (1991) Purification and characterization of acetoin: 2, 6-dichlorophenolindophenol oxidoreductase, dihydrolipoamide dehydrogenase, and dihydrolipoamide acetyltransferase of the Pelobacter carbinolicus acetoin dehydrogenase enzyme system. J Bacteriol 173(2):757–767. https://doi.org/10.1128/jb.173.2.757-767.1991
Hung KC, Nguyen NT, Sun YL, Huang SL (2019) Bio-Fenton reaction involved in the cleavage of the ethoxylate chain of nonionic surfactants by dihydrolipoamide dehydrogenase from pseudomonas nitroreducens TX1. Sci Rep 9:6827. https://doi.org/10.1038/s41598-019-43266-8
Araújo WL, Trofimova L, Mkrtchyan G, Steinhauser D, Krall L, Graf A, Fernie AR, Bunik VI (2013) On the role of the mitochondrial 2-oxoglutarate dehydrogenase complex in amino acid metabolism. Amino Acids 44(2):683–700. https://doi.org/10.1007/s00726-012-1392-x
Nemeria NS, Gerfen G, Yang L, Zhang X (1859) Jordan F (2018) evidence for functional and regulatory cross-talk between the tricarboxylic acid cycle 2-oxoglutarate dehydrogenase complex and 2-oxoadipate dehydrogenase on the l-lysine, l-hydroxylysine and l-tryptophan degradation pathways from studies in vitro. Biochim Biophys Acta Bioenerg 9:932–939. https://doi.org/10.1016/j.bbabio.2018.05.001
Shinohara M, Sato N, Kurinami H, Takeuchi D, Takeda S, Shimamura M, Yamashita T, Uchiyama Y, Rakugi H, Morishita R (2010) Reduction of brain β-amyloid (Aβ) by fluvastatin, a hydroxymethylglutaryl-CoA reductase inhibitor, through increase in degradation of amyloid precursor protein C-terminal fragments (APP-CTFs) and Aβ clearance. J Biol Chem 285(29):22091–22102. https://doi.org/10.1074/jbc.M110.102277
Jaskiewicz J, Zhao Y, Hawes JW, Shimomura Y, Crabb DW, Harris RA (1996) Catabolism of isobutyrate by colonocytes. Arch Biochem Biophys 327(2):265–270. https://doi.org/10.1006/abbi.1996.0120
Pan Y, Yang J, Gong Y, Li X, Hu H (2017) 3-Hydroxyisobutyryl-CoA hydrolase involved in isoleucine catabolism regulates triacylglycerol accumulation in Phaeodactylum tricornutum. Phil Trans R Soc B Biol Sci 372:20160409. https://doi.org/10.1098/rstb.2016.0409
Large PJ, Robertson A (1988) The subcellular location of 4-aminobutyrate aminotransferase in Candida boidinii and its probable role in the breakdown of putrescine and spermidine. Yeast 4(2):149–153. https://doi.org/10.1002/yea.320040209
Kim YT, Churchich JE (1991) 4-Aminobutyrate aminotransferase: identification of lysine residues connected with catalytic activity. Biochim Biophys Acta Protein Struct Mol Enzymol 1077(2):187–191. https://doi.org/10.1016/0167-4838(91)90057-7
Wang J, Wang C, Li Q, Shen M, Bai P, Li J, Lin Y, Gan N, Li T, Zhao J (2019) Microcystin-LR degradation and gene regulation of microcystin-degrading Novosphingobium sp. THN1 at different carbon concentrations. Front Microbiol 10(1750). https://doi.org/10.3389/fmicb.2019.01750
Dommes V, Baumgart C, Kunau W (1981) Degradation of unsaturated fatty acids in peroxisomes. Existence of a 2, 4-dienoyl-CoA reductase pathway. J Biol Chem 256(16):8259–8262. https://doi.org/10.1016/S0021-9258(19)68833-2
Gerhardt B (1992) Fatty acid degradation in plants. Prog Lipid Res 31(4):417–446. https://doi.org/10.1016/0163-7827(92)90004-3
Zwierz K, Gindzienski A, Glowacka D, Porowski T (1981) The degradation of glycoconjugates in the human gastric mucous membrane. Acta Med Acad Sci Hungaricae 38(2):145–152
De Gasperi R, Daniel PF, Warren CD (1992) A human lysosomal alpha-mannosidase specific for the core of complex glycans. J Biol Chem 267(14):9706–9712. https://doi.org/10.1016/S0021-9258(19)50148-X
Wang Y, Zhang J, Wu Y, Wang L, Jia Z (2017) Effects of soil bacteria inoculation in spray seeding matrix on photosynthesis characteristics and chlorophyll fluorescence parameters of Amorpha fruticose. Res Environ Sci 30(6):902–910
Wu Y, Zhang J, Guo X, Wang Y, Wang Q (2017) Isolation and characterisation of a rock solubilising fungus for application in mine-spoil reclamation. Eur J Soil Biol 81:76–82. https://doi.org/10.1016/j.ejsobi.2017.06.011
Wang G, Deng H, Nie L, Wu Y, Zhang J (2018) Mechanism of limestone corrosion by Gongronella butleri NL-15. Chinese J Appl Environ Biol 24:374–378. https://doi.org/10.19675/j.cnki.1006-687x.2017.05018
Li C, Jia Z, Zhai L, Zhang B, Peng X, Liu X, Zhang J (2021) Effects of mineral-solubilizing microorganisms on root growth, soil nutrient content, and enzyme activities in the rhizosphere soil of Robinia pseudoacacia. Forests 12(1):60. https://doi.org/10.3390/f12010060