Millipede gut-derived microbes as a potential source of cellulolytic enzymes

. 2023 Apr 26 ; 39 (7) : 169. [epub] 20230426

Jazyk angličtina Země Německo Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37186294

Grantová podpora
17-22572S Czech Science Foundation
CENAKVA (LM2018099) Ministry of Education, Youth and Sports of the Czech Republic

Odkazy

PubMed 37186294
DOI 10.1007/s11274-023-03620-5
PII: 10.1007/s11274-023-03620-5
Knihovny.cz E-zdroje

Lignocellulose biomass has recently been considered a cost-effective and renewable energy source within circular economy management. Cellulases are important key enzymes for simple, fast, and clean biomass decomposition. The intestinal tract of millipedes is the environment which can provide promising microbial strains with cellulolytic potential. In the present study, we used the tropical millipede Telodeinopus aoutii as an experimental organism. Within a feeding test in which millipedes were fed with oak and maple leaf litter, we focused on isolating culturable cellulolytic microbiota from the millipede gut. Several growth media selecting for actinobacteria, bacteria, and fungi have been used to cultivate microbial strains with cellulolytic activities. Our results showed that oak-fed millipedes provided a higher number of culturable bacteria and a more diversified microbial community than maple-fed ones. The screening for cellulolytic activity using Congo red revealed that about 30% of bacterial and fungal phylotypes isolated from the gut content of T. aoutii, produced active cellulases in vitro. Actinobacteria Streptomyces and Kitasatospora were the most active cellulolytic genera on Congo red test. In contrast, fungi Aspergillus, Penicillium, Cheatomium, Clonostachys, and Trichoderma showed the highest protein-specific cellulase activity quantified by 4-Methylumbelliferyl β-D-cellobioside (4-MUC). Our findings provide a basis for future research on the enzyme activities of microbes isolated from the digestive tracts of invertebrates and their biocatalytic role in biomass degradation.

Zobrazit více v PubMed

Affandi M, Trikurniadewi N, Abidin A, Khiftiyah A, Sari S, Ibrahim S, Jannah M, Masrurin A, Makrifah R (2021) Enzymatic activity of bacteria isolated from the gut of Cylindroiulus sp.: future prospect for decomposing agent. IOP Publishing, Bristol, p 012042

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2 PubMed DOI

Bani A, Pioli S, Ventura M, Panzacchi P, Borruso L, Tognetti R, Tonon G, Brusetti L (2018) The role of microbial community in the decomposition of leaf litter and deadwood. Appl Soil Ecol 126:75–84. https://doi.org/10.1016/j.apsoil.2018.02.017 DOI

Baumann P, Moran NA (1997) Non-cultivable microorganisms from symbiotic associations of insects and other hosts. Antonie Leeuwenhoek 72:39–48. https://doi.org/10.1023/A:1000239108771 PubMed DOI

Belmont-Montefusco EL, Nacif-Marcal L, Assunção END, Hamada N, Nunes-Silva CG (2020) Cultivable cellulolytic fungi isolated from the gut of Amazonian aquatic insects. Acta Amazon 50:346–354. https://doi.org/10.1590/1809-4392202000902 DOI

Book AJ, Lewin GR, McDonald BR, Takasuka TE, Wendt-Pienkowski E, Doering DT, Suh S, Raffa KF, Fox BG, Currieet CR (2016) Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression. PLoS Biol 14:e1002475. https://doi.org/10.1371/journal.pbio.1002475 PubMed DOI PMC

Boschker H, Cappenberg TE (1994) A sensitive method using 4-methylumbelliferyl-β-cellobiose as a substrate to measure (1,4)-β-glucanase activity in sediments. Appl Environ Microb 60:3592–3596. https://doi.org/10.1128/aem.60.10.3592-3596.1994 DOI

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3 PubMed DOI

Bredon M, Herran B, Lheraud B, Bertaux J, Grève P, Moumen B, Bouchon D (2019) Lignocellulose degradation in isopods: new insights into the adaptation to terrestrial life. BMC Genomics 20:1–14. https://doi.org/10.1186/s12864-019-5825-8 DOI

Brown SP, Brogden M, Cortes C, Tucker AE, VandeVoort AR, Snyder BA (2021) Investigating the effects of nitrogen deposition and substrates on the microbiome and mycobiome of the millipede Cherokia georgiana georgiana (Diplopoda: Polydesmida). Soil Biol Biochem 159:108285. https://doi.org/10.1016/j.soilbio.2021.108285 DOI

Brucker RM, Bordenstein SR (2012) The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution 66:349–362. https://doi.org/10.1111/j.1558-5646.2011.01454.x PubMed DOI

Bulakhov A, Gusakov A, Chekushina A, Satrutdinov A, Koshelev A, Matys VY, Sinitsyn A (2016) Isolation of homogeneous polysaccharide monooxygenases from fungal sources and investigation of their synergism with cellulases when acting on cellulose. Biochemistry 81:530–537. https://doi.org/10.1134/S0006297916050102 PubMed DOI

Byzov BA (2006) Intestinal microbiota of millipedes. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, New York, pp 89–114 DOI

Byzov B, Thanh VN, Babjeva I (1993a) Yeasts associated with soil invertebrates. Biol Fertil Soils 16:183–187. https://doi.org/10.1007/BF00361405 DOI

Byzov B, Zenova G, Babkina N, Dobrovolskaya T, Tretjakova E (1993b) Actinomycetes in the food, gut and faeces of soil millipede, Pahyiulus flavipes CL Koch. Mikrobiologia 62:916–927

Byzov B, Chernjakovskaya T, Zenova G, Dobrovolskaya T (1996) Bacterial communities associated with soil diplopods. Pedobiologia 40:67–79

Cafaro MJ (2005) Eccrinales (Trichomycetes) are not fungi, but a clade of protists at the early divergence of animals and fungi. Mol Phylogenet Evol 35:21–34. https://doi.org/10.1016/j.ympev.2004.12.019 PubMed DOI

Carreiro M, Sinsabaugh R, Repert D, Parkhurst D (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365. https://doi.org/10.1890/0012-9658(2000)081[2359:MESELD]2.0.CO;2 DOI

Cazemier AE, Verdoes JC, Reubsaet FA, Hackstein JH, van der Drift C, Den Camp HJO (2003) Promicromonospora pachnodae sp. nov., a member of the (hemi)cellulolytic hindgut flora of larvae of the scarab beetle Pachnoda marginata. Antonie Leeuwenhoek 83:135–148. https://doi.org/10.1023/A:1023325817663 DOI

Ceja-Navarro JA, Karaoz U, Bill M, Hao Z, White RA, Arellano A, Ramanculova L, Filley TR, Berry TD, Conrad ME (2019) Gut anatomical properties and microbial functional assembly promote lignocellulose deconstruction and colony subsistence of a wood-feeding beetle. Nat Microbiol 4:864–875. https://doi.org/10.1038/s41564-019-0384-y PubMed DOI

Chernoglazov VM, Jafarova AN, Klyosov AA (1989) Continuous photometric determination of endo-1, 4-β-D-glucanase (cellulase) activity using 4-methylumbelliferyl-β-D-cellobioside as a substrate. Anal Biochem 179:186–189. https://doi.org/10.1016/0003-2697(89)90222-4 PubMed DOI

Chevrette MG, Carlson CM, Ortega HE, Thomas C, Ananiev GE, Barns KJ, Book AJ, Cagnazzo J, Carlos C, Flanigan W (2019) The antimicrobial potential of Streptomyces from insect microbiomes. Nat Commun 10:1–11. https://doi.org/10.1038/s41467-019-08438-0 DOI

Corrêa TLR, Dos Santos LV, Pereira GAG (2016) AA9 and AA10: from enigmatic to essential enzymes. Appl Microbiol Biotechnol 100:9–16. https://doi.org/10.1007/s00253-015-7040-0 PubMed DOI

Dangerfield J, Milner AE (1993) Ingestion and assimilation of leaf litter in some tropical millipedes. J Zool 229:683–693. https://doi.org/10.1111/j.1469-7998.1993.tb02664.x DOI

Degelmann DM, Kolb S, Dumont M, Murrell JC, Drake HL (2009) Enterobacteriaceae facilitate the anaerobic degradation of glucose by a forest soil. FEMS Microbiol Ecol 68:312–319. https://doi.org/10.1111/j.1574-6941.2009.00681.x PubMed DOI

Drula E, Garron M-L, Dogan S, Lombard V, Henrissat B, Terrapon N (2022) The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res 50:D571–D577. https://doi.org/10.1093/nar/gkab1045 PubMed DOI

Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853. https://doi.org/10.1093/nar/17.19.7843 PubMed DOI PMC

Engel P, Moran NA (2013) The gut microbiota of insects–diversity in structure and function. FEMS Microbiol Rev 37:699–735. https://doi.org/10.1111/1574-6976.12025 PubMed DOI

Ezeilo UR, Zakaria II, Huyop F, Wahab RA (2017) Enzymatic breakdown of lignocellulosic biomass: the role of glycosyl hydrolases and lytic polysaccharide monooxygenases. Biotechnol Biotechnol Equip 31:647–662. https://doi.org/10.1080/13102818.2017.1330124 DOI

Garlapati VK, Chandel AK, Kumar SJ, Sharma S, Sevda S, Ingle AP, Pant D (2020) Circular economy aspects of lignin: towards a lignocellulose biorefinery. Renew Sust Energ Rev 130:109977. https://doi.org/10.1016/j.rser.2020.109977 DOI

Geib SM, Jimenez-Gasco MDM, Carlson JE, Tien M, Hoover K (2009) Effect of host tree species on cellulase activity and bacterial community composition in the gut of larval Asian longhorned beetle. Environ Entomol 38:686–699. https://doi.org/10.1603/022.038.0320 PubMed DOI

Gil J, Campelo-Diez A (2003) Candicidin biosynthesis in Streptomyces griseus. Appl Microbiol Biotechnol 60:633–642. https://doi.org/10.1007/s00253-002-1163-9 PubMed DOI

Glukhova AA, Karabanova AA, Yakushev AV, Semenyuk II, Boykova YV, Malkina ND, Efimenko TA, Ivankova TD, Terekhova LP, Efremenkova OV (2018) Antibiotic activity of actinobacteria from the digestive tract of millipede Nedyopus dawydoffiae (Diplopoda). Antibiotics 7:94. https://doi.org/10.3390/antibiotics7040094 PubMed DOI PMC

Hao C, de Jonge N, Zhu D, Feng L, Zhang B, Chen T-W, Wu D, Nielsen JL (2022) Food origin influences microbiota and stable isotope enrichment profiles of cold-adapted Collembola (Desoria ruseki). Front Microbiol. https://doi.org/10.3389/fmicb.2022.1030429 PubMed DOI PMC

Harir M, Bendif H, Bellahcene M, Fortas Z, Pogni R (2018) Streptomyces secondary metabolites. In: Enany S (ed) Basic biology and applications of actinobacteria. IntechOpen, London, pp 99–122

Hasaneen M, El-Sayed A, Sabry S (2018) Identification, characterization and optimized antimicrobial production of Streptomyces thinghirensis isolate. J Agric Chem Biotechnol 9:263–268. https://doi.org/10.21608/jacb.2018.36315 DOI

Hoang DT, Chernomor O, Von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281 PubMed DOI

Homolka L, Lisá L, Eichlerová I, Nerud F (2001) Cryopreservation of basidiomycete strains using perlite. J Microbiol Methods 47:307–313. https://doi.org/10.1016/S0167-7012(01)00338-4 PubMed DOI

Horváthová T, Šustr V, Chroňáková A, Semanová S, Lang K, Carsten D, Hubáček T, Ardestani MM, Lara AC, Brune A, Šimek M (2021) Methanogenesis in the digestive tracts of the tropical millipedes Archispirostreptus gigas (Diplopoda, Spirostreptidae) and Epibolus pulchripes (Diplopoda, Pachybolidae). Appl Environ Microb 87:e00614-e621. https://doi.org/10.1128/AEM.00614-21 DOI

Ineson P, Anderson J (1985) Aerobically isolated bacteria associated with the gut and faeces of the litter feeding macroarthropods Oniscus asellus and Glomeris marginata. Soil Biol Biochem 17:843–849. https://doi.org/10.1016/0038-0717(85)90145-2 DOI

Jarosz J, Kania G (2000) The question of whether gut microflora of the millipede Ommatoiulus sabulosus could function as a threshold to food infections. Pedobiologia 44:705–708. https://doi.org/10.1078/S0031-4056(04)70083-9 DOI

Jasalavich CA, Ostrofsky A, Jellison J (2000) Detection and identification of decay fungi in spruce wood by restriction fragment length polymorphism analysis of amplified genes encoding rRNA. Appl Environ Microb 66:4725–4734. https://doi.org/10.1128/AEM.66.11.4725-4734.2000 DOI

Kalyaanamoorthy S, Minh BQ, Wong TK, Von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285 PubMed DOI PMC

Kane MD (1997) Microbial fermentation in insect guts. In: White BA (ed) Mackie R I. Gastrointestinal microbiology, Springer, pp 231–265

Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30. https://doi.org/10.1093/nar/28.1.27 PubMed DOI PMC

Keiser AD, Warren R, Filley T, Bradford MA (2021) Signatures of an abiotic decomposition pathway in temperate forest leaf litter. Biogeochemistry 153:177–190. https://doi.org/10.1007/s10533-021-00777-9 DOI

Koeck DE, Pechtl A, Zverlov VV, Schwarz WH (2014) Genomics of cellulolytic bacteria. Curr Opin Biotechnol 29:171–183. https://doi.org/10.1016/j.copbio.2014.07.002 PubMed DOI

König H (2006) Bacillus species in the intestine of termites and other soil invertebrates. J Appl Microbiol 101:620–627. https://doi.org/10.1111/j.1365-2672.2006.02914.x PubMed DOI

König H, Fröhlich J (2006) Diversity and lignocellulolytic activities of cultured microorganisms. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, New York, pp 271–301 DOI

König H, Li L, Fröhlich J (2013) The cellulolytic system of the termite gut. Appl Microbiol Biotechnol 97:7943–7962. https://doi.org/10.1007/s00253-013-5119-z PubMed DOI

Koubová A, Chroňáková A, Pižl V, Sánchez-Monedero MA, Elhottová D (2015) The effects of earthworms Eisenia spp. on microbial community are habitat dependent. Eur J Soil Biol 68:42–55. https://doi.org/10.1016/j.ejsobi.2015.03.004 DOI

Kyselková M, Chroňáková A, Volná L, Nĕmec J, Ulmann V, Scharfen J, Elhottová D (2012) Tetracycline resistance and presence of tetracycline resistance determinants tet (V) and tap in rapidly growing mycobacteria from agricultural soils and clinical isolates. Microbes Environ. https://doi.org/10.1264/jsme2.ME12028 PubMed DOI PMC

Lemoine F, Domelevo Entfellner J-B, Wilkinson E, Correia D, Dávila Felipe M, De Oliveira T, Gascuel O (2018) Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 556:452–456. https://doi.org/10.1038/s41586-018-0043-0 PubMed DOI PMC

Loqman S, Bouizgarne B, Barka EA, Clément C, Von Jan M, Spröer C, Klenk H-P, Ouhdouch Y (2009) Streptomyces thinghirensis sp. nov., isolated from rhizosphere soil of Vitis vinifera. Int J Syst Evol Microbiol 59:3063–3067. https://doi.org/10.1099/ijs.0.008946-0 PubMed DOI

Mwabvu T, Lamb J, Slotow R, Hamer M, Barraclough D (2013) Is millipede taxonomy based on gonopod morphology too inclusive? Observations on genetic variation and cryptic speciation in Bicoxidens flavicollis (Diplopoda: Spirostreptida: Spirostreptidae): Myriapoda. Afr Invertebr 54:349–356 DOI

Nardi JB, Bee CM, Taylor SJ (2016) Compartmentalization of microbial communities that inhabit the hindguts of millipedes. Arthropod Struct Dev 45:462–474. https://doi.org/10.1016/j.asd.2016.08.007 PubMed DOI

Nguyen Duc T, Byzov B, Zenova G, Zvyagintsev D (1996) Antagonistic properties of actinomycetes associated with the intestinal tract of soil invertebrates. Moscow University Soil Science Bulletin C/c of Vestnik-Moskovskii Universitet Pochvovedenie 51:28–34

Nguyen L-T, Schmidt HA, Von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300 PubMed DOI

Oravecz O, Nyiro G, Márialigeti K (2002) A molecular approach in the analysis of the faecal bacterial community in an African millipede belonging to the family Spirostreptidae (Diplopoda). Eur J Soil Biol 38:67–70. https://doi.org/10.1016/S1164-5563(01)01128-1 DOI

Pramanik R, Sarkar K, Joy V (2001) Efficiency of detritivore soil arthropods in mobilizing nutrients from leaf litter. Trop Ecol 42:51–58

Prem Anand AA, Vennison SJ, Sankar SG, Gilwax Prabhu DI, Vasan PT, Raghuraman T, Jerome Geoffrey C, Vendan SE (2010) Isolation and characterization of bacteria from the gut of Bombyx mori that degrade cellulose, xylan, pectin and starch and their impact on digestion. J Insect Sci 10:107. https://doi.org/10.1673/031.010.10701 PubMed DOI PMC

Prillinger H, König H (2006) The intestinal yeasts. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, New York, pp 319–334 DOI

Ramanathan B, Alagesan P (2012) Isolation, characterization and role of gut bacteria of three different millipede species. Environ J Sci Res 3:55–61

Roa JJH, Virella CR, Cafaro MJ (2009) First survey of arthropod gut fungi and associates from Vieques, Puerto Rico. Mycologia 101:896–903. https://doi.org/10.3852/08-187 DOI

Sabbadin F, Hemsworth GR, Ciano L, Henrissat B, Dupree P, Tryfona T, Marques RD, Sweeney ST, Besser K, Elias L (2018) An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion. Nat Commun 9:1–12. https://doi.org/10.1038/s41467-018-03142-x DOI

Sajith S, Priji P, Sreedevi S, Benjamin S (2016) An overview on fungal cellulases with an industrial perspective. J Nutr Food Sci 6:461. https://doi.org/10.4172/2155-9600.1000461 DOI

Sardar P, Šustr V, Chroňáková A, Lorenc F (2022a) Metatranscriptomic holobiont analysis of carbohydrate active enzymes in the millipede Telodeinopus aoutii (Diplopoda, Spirostreptida). Front Ecol Evol 10:931986. https://doi.org/10.3389/fevo.2022.931986 DOI

Sardar P, Šustr V, Chroňáková A, Lorenc F, Faktorová L (2022b) De novo metatranscriptomic exploration of gene function in the millipede holobiont. Sci Rep 12:1–15. https://doi.org/10.1038/s41598-022-19565-y DOI

Sazci A, Erenler K, Radford A (1986) Detection of cellulolytic fungi by using Congo red as an indicator: a comparative study with the dinitrosalicyclic acid reagent method. J Appl Bacteriol 61:559–562. https://doi.org/10.13140/RG.2.1.1109.2888 DOI

Schapheer C, Pellens R, Scherson R (2021) Arthropod–microbiota integration: its importance for ecosystem conservation. Front Microbiol 12:2094. https://doi.org/10.3389/fmicb.2021.702763 DOI

Sharma D, Joshi B, Bhatt MR, Joshi J, Malla R, Bhattarai T, Sreerama L (2015) Isolation of cellulolytic organisms from the gut contents of termites native to Nepal and their utility in saccharification and fermentation of lignocellulosic biomass. J Biomass Biofuel 2:11–20. https://doi.org/10.11159/jbb.2015.002 DOI

Sidar A, Albuquerque ED, Voshol GP, Ram AF, Vijgenboom E, Punt PJ (2020) Carbohydrate binding modules: diversity of domain architecture in amylases and cellulases from filamentous microorganisms. Front Bioeng Biotechnol 8:871. https://doi.org/10.3389/fbioe.2020.00871 PubMed DOI PMC

Sigling S (2010) Professional breeders series, Millipedes. Chimaira, Frankfurt am Main

Soni SK, Sharma A, Soni R (2018) Cellulases: role in lignocellulosic biomass utilization. In: Walker JM (ed) Methods in molecular biology. Springer, Cham, pp 3–23

Straigytė L, Jurkšienė G, Armolaitis K (2009) Decomposition of oak and maple leaf litters: comparative study of native and alien species. Sustain Dev for 4:196–200

Šuchová K, Fehér C, Ravn JL, Bedő S, Biely P, Geijer C (2022) Cellulose-and xylan-degrading yeasts: Enzymes, applications and biotechnological potential. Biotechnol Adv 59:107981. https://doi.org/10.1016/j.biotechadv.2022.107981 PubMed DOI

Suh S-O, Blackwell M, Kurtzman CP, Lachance M-A (2006) Phylogenetics of Saccharomycetales, the ascomycete yeasts. Mycologia 98:1006–1017. https://doi.org/10.1080/15572536.2006.11832629 PubMed DOI

Šustr V, Semanová S, Rost-Roszkowska M, Tajovský K, Sosinka A, Kaszuba F (2020a) Enzymatic activities in the digestive tract of spirostreptid and spirobolid millipedes (Diplopoda: Spirostreptida and Spirobolida). Comp Biochem Phys B 241:110388. https://doi.org/10.1016/j.cbpb.2019.110388 DOI

Šustr V, Šimek M, Faktorová L, Macková J, Tajovský K (2020b) Release of greenhouse gases from millipedes as related to food, body size, and other factors. Soil Biol Biochem 144:107765. https://doi.org/10.1016/j.soilbio.2020.107765 DOI

Szabo I, Jager K, Contreras E, Marialigeti K, Dzingov A, Barabas G, Pobozsny M (1983) Composition and properties of the external and internal microflora of millipedes (Diplopoda). In: Lebrun P, Andre H M, De Medts A, Gregoire-Wibo C, Wauthy G (eds), Proceedings of the Eighth International Colloquium on Soil Zoology Dieu-Brichart Ottignies-Louvain-la-Neuve France, pp 197–206

Szabo I M, Nasser E-G, Striganova B, Rakhmo Y R, Jager K, Heydrich M (1992) Interactions among millipedes (Diplopoda) and their intestinal bacteria. Ber Nat-Med Ver Innsbruck

Taylor EC (1982) Role of aerobic microbial populations in cellulose digestion by desert millipedes. Appl Environ Microbiol 44:281–291 PubMed DOI PMC

Teather RM, Wood PJ (1982) Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microb 43:777–780 DOI

ter Braak C J F, Šmilauer P (2012) Canoco reference manual and user's guide: software for ordination, version 5.0, Microcomputer Power, Ithaca, USA, 496pp

Thapa S, Mishra J, Arora N, Mishra P, Li H, Bhatti S, Zhou S (2020) Microbial cellulolytic enzymes: diversity and biotechnology with reference to lignocellulosic biomass degradation. Rev Environ Sci Biotechnol 19:621–648. https://doi.org/10.1007/s11157-020-09536-y DOI

Tokuda G (2019) Plant cell wall degradation in insects: recent progress on endogenous enzymes revealed by multi-omics technologies. Adv Insect Physiol 57:97–136. https://doi.org/10.1016/bs.aiip.2019.08.001 DOI

Tret’yakova E, Dobrovol’skaya T, Byzov B, Zvyagintsev D (1996) Bacterial communities associated with soil invertebrates. Microbiology 65:91–97

Velvizhi G, Balakumar K, Shetti NP, Ahmad E, Pant KK, Aminabhavi TM (2022) Integrated biorefinery processes for conversion of lignocellulosic biomass to value added materials: Paving a path towards circular economy. Bioresour Technol 343:126151. https://doi.org/10.1016/j.biortech.2021.126151 PubMed DOI

Vongsuvanlert V, Tani Y (1989) Xylitol production by a methanol yeast, Candida boidinii (Kloeckera sp.) No. 2201. J Ferment Bioeng 67:35–39. https://doi.org/10.1016/0922-338X(89)90083-4 DOI

Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632. https://doi.org/10.1146/annurev-ento-112408-085319 PubMed DOI

Wellington E, Toth I (1994) Actinomycetes. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis: part II. Microbiological and biochemical properties, SSSA book series no 5. Soil Science Society of America, Madison, pp 269–290

White MM, Cafaro MJ, Lichtwardt RW (2000) Arthropod gut fungi from Puerto Rico and summary of tropical Trichomycetes worldwide. Caribb J Sci 36:210–220

Wright K (1979) Trichomycetes and oxyuroid nematodes in the millipede, Narceus annularis. Proc Helminthol Soc Wash 46:213–223

Wu M, Nerinckx W, Piens K, Ishida T, Hansson H, Sandgren M, Ståhlberg J (2013) Rational design, synthesis, evaluation and enzyme–substrate structures of improved fluorogenic substrates for family 6 glycoside hydrolases. FEBS J 280:184–198. https://doi.org/10.1111/febs.12060 PubMed DOI

Žifčáková L, Baldrian P (2012) Fungal polysaccharide monooxygenases: new players in the decomposition of cellulose. Fungal Ecol 5:481–489. https://doi.org/10.1016/j.funeco.2012.05.001 DOI

Zimmer M (1999) Combined methods for the determination of lignin and cellulose in leaf litter. Sci Soils 4:14–21. https://doi.org/10.1007/s10112-999-0002-x DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace