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Journal of Microbiology

, Volume 57, Issue 10, pp 865–873 | Cite as

Antarctic tundra soil metagenome as useful natural resources of cold-active lignocelluolytic enzymes

  • Han Na Oh
  • Doyoung Park
  • Hoon Je Seong
  • Dockyu KimEmail author
  • Woo Jun SulEmail author
Microbial Ecology and Environmental Microbiology

Abstract

Lignocellulose composed of complex carbohydrates and aromatic heteropolymers is one of the principal materials for the production of renewable biofuels. Lignocellulose-degrading genes from cold-adapted bacteria have a potential to increase the productivity of biological treatment of lignocellulose biomass by providing a broad range of treatment temperatures. Antarctic soil metagenomes allow to access novel genes encoding for the cold-active lignocellulose-degrading enzymes, for biotechnological and industrial applications. Here, we investigated the metagenome targeting cold-adapted microbes in Antarctic organic matter-rich soil (KS 2-1) to mine lignolytic and celluloytic enzymes by performing single molecule, real-time metagenomic (SMRT) sequencing. In the assembled Antarctic metagenomic contigs with relative long reads, we found that 162 (1.42%) of total 11,436 genes were annotated as carbohydrate-active enzymes (CAZy). Actinobacteria, the dominant phylum in this soil’s metagenome, possessed most of candidates of lignocellulose catabolic genes like glycoside hydrolase families (GH13, GH26, and GH5) and auxiliary activity families (AA7 and AA3). The predicted lignocellulose degradation pathways in Antarctic soil metagenome showed synergistic role of various CAZyme harboring bacterial genera including Streptomyces, Streptosporangium, and Amycolatopsis. From phylogenetic relationships with cellular and environmental enzymes, several genes having potential for participating in overall lignocellulose degradation were also found. The results indicated the presence of lignocellulose-degrading bacteria in Antarctic tundra soil and the potential benefits of the lignocelluolytic enzymes as candidates for cold-active enzymes which will be used for the future biofuel-production industry.

Keywords

metagenomics lignocellulose degradation SMRT sequencing CAZy cold-active enzymes Antarctica 

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Notes

Acknowledgements

This research was supported by a grant to the Korea Polar Research Institute (PE19090) and by the Collaborative Genome Program of the Korea Institute of Marine Science and Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (MOF) (No. 20180430).

References

  1. Aislabie, J.M., Jordan, S., and Barker, G.M. 2008. Relation between soil classification and bacterial diversity in soils of the Ross Sea region, Antarctica. Geoderma 144, 9–20.CrossRefGoogle Scholar
  2. Caporaso, J.G., Bittinger, K., Bushman, F.D., DeSantis, T.Z., Andersen, G.L., and Knight, R. 2009. Pynast: A flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266–267.CrossRefGoogle Scholar
  3. Chin, C.S., Alexander, D.H., Marks, P., Klammer, A.A., Drake, J., Heiner, C., Clum, A., Copeland, A., Huddleston, J., and Eichler, E.E. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563–569.CrossRefGoogle Scholar
  4. Cole, J.R., Wang, Q., Fish, J.A., Chai, B., McGarrell, D.M., Sun, Y., Brown, C.T., Porras-Alfaro, A., Kuske, C.R., and Tiedje, J.M. 2014. Ribosomal database project: Data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, D633–642.CrossRefGoogle Scholar
  5. Devasia, S. and Nair, A.J. 2016. Screening of potent laccase producing organisms based on the oxidation pattern of different phenolic substrates. Int. J. Curr. Microbiol. Appl. Sci. 5, 127–137.CrossRefGoogle Scholar
  6. Devi, P., Kandasamy, S., Chendrayan, K., and Uthandi, S. 2016. Laccase producing Streptomyces bikiniensis CSC 12 isolated from compost. J. Microbiol. Biotechnol. Food Sci. 6, 794–798.CrossRefGoogle Scholar
  7. Dey, G., Palit, S., Banerjee, R., and Maiti, B. 2002. Purification and characterization of maltooligosaccharide-forming amylase from Bacillus circulans GRS 313. J. Ind. Microbiol. Biotechnol. 28, 193–200.CrossRefGoogle Scholar
  8. Dhar, H., Kasana, R.C., Dutt, S., and Gulati, A. 2015. Cloning and expression of low temperature active endoglucanase EG5C from Paenibacillus sp. IHB B 3084. Int. J. Biol. Macromol. 81, 259–266.CrossRefGoogle Scholar
  9. Ducros, V., Czjzek, M., Belaich, A., Gaudin, C., Fierobe, H.P., Belaich, J.P., Davies, G.J., and Haser, R. 1995. Crystal structure of the catalytic domain of a bacterial cellulase belonging to family 5. Structure 3, 939–949.CrossRefGoogle Scholar
  10. Edgar, R.C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.CrossRefGoogle Scholar
  11. Foong, F., Hamamoto, T., Shoseyov, O., and Doi, R.H. 1991. Nucleotide sequence and characteristics of endoglucanase gene engB from Clostridium cellulovorans. J. Gen. Microbiol. 137, 1729–1736.CrossRefGoogle Scholar
  12. Garsoux, G., Lamotte, J., Gerday, C., and Feller, G. 2004. Kinetic and structural optimization to catalysis at low temperatures in a psychrophilic cellulase from the antarctic bacterium Pseudoalteromonas haloplanktis. Biochem. J. 384, 247–253.CrossRefGoogle Scholar
  13. Goldstein, I.S. 1981. Composition of biomass. In Goldstein, I.S. (ed.), Organic Chemicals from Biomass, pp. 9–19. CRC Press Inc., Boca Raton, FL, USA.Google Scholar
  14. Granja-Travez, R.S., Wilkinson, R.C., Persinoti, G.F., Squina, F.M., Fülöp, V., and Bugg, T.D. 2018. Structural and functional characterisation of multi-copper oxidase CueO from lignin-degrading bacterium Ochrobactrum sp. reveal its activity towards lignin model compounds and lignosulfonate. FEBS J. 285, 1684–1700.CrossRefGoogle Scholar
  15. Huerta-Cepas, J., Forslund, K., Coelho, L.P., Szklarczyk, D., Jensen, L.J., von Mering, C., and Bork, P. 2017. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol. Biol. Evol. 34, 2115–2122.CrossRefGoogle Scholar
  16. Iyo, A.H. and Forsberg, C.W. 1999. A cold-active glucanase from the ruminal Bacteriumfibrobacter succinogenes S85. Appl. Environ. Microbiol. 65, 995–998.PubMedPubMedCentralGoogle Scholar
  17. Jiménez, D.J., de Lima Brossi, M.J., Schückel, J., Kračun, S.K., Willats, W.G.T., and van Elsas, J.D. 2016. Characterization of three plant biomass-degrading microbial consortia by metagenomics-and metasecretomics-based approaches. Appl. Microbiol. Biotechnol. 100, 10463–10477.CrossRefGoogle Scholar
  18. Johnson, E. 2016. Integrated enzyme production lowers the cost of cellulosic ethanol. Biofuel Bioprod. Biorefin. 10, 164–174.CrossRefGoogle Scholar
  19. Kikani, B. and Singh, S. 2011. Single step purification and characterization of a thermostable and calcium independent α-amylase from Bacillus amyloliquifaciens TSWK1-1 isolated from Tulsi Shyam hot spring reservoir, Gujarat (India). Int. J. Biol. Macromol. 48, 676–681.CrossRefGoogle Scholar
  20. Kim, J.H., Ahn, I.Y., Lee, K.S., Chung, H., and Choi, H.G. 2007. Vegetation of Barton peninsula in the neighbourhood of King Sejong Station (King George Island, maritime Antarctic). Polar. Biol. 30, 903–916.CrossRefGoogle Scholar
  21. Kim, S.C., Kim, J.S., Hong, B.R., Hong, S.G., Kim, J.H., and Lee, K.S. 2016. Assembly processes of moss and lichen community with snow melting at the coastal region of the Barton peninsula, maritime Antarctic. J. Ecol. Environ. 40, 8.CrossRefGoogle Scholar
  22. Kim, C., Lorenz, W.W., Hoopes, J.T., and Dean, J.F. 2001. Oxidation of phenolate siderophores by the multicopper oxidase encoded by the Escherichia coli yacK gene. J. Bacteriol. 183, 4866–4875.CrossRefGoogle Scholar
  23. Kuddus, M. 2014. Bio-statistical approach for optimization of cold-active α-amylase production by novel psychrotolerant M. foliorum GA2 in solid state fermentation. Biocatal. Agric. Biotechnol. 3, 175–181.CrossRefGoogle Scholar
  24. Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. 2018. Mega X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549.CrossRefGoogle Scholar
  25. Lee, Y.I., Lim, H.S., and Yoon, H.I. 2004. Geochemistry of soils of king george island, South Shetland Islands, West Antarctica: Implications for pedogenesis in cold polar regions. Geochim. Cosmochim. Acta. 68, 4319–4333.CrossRefGoogle Scholar
  26. Levasseur, A., Drula, E., Lombard, V., Coutinho, P.M., and Henrissat, B. 2013. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol. Biofuels 6, 41.CrossRefGoogle Scholar
  27. Li, P.E., Lo, C.C., Anderson, J.J., Davenport, K.W., Bishop-Lilly, K.A., Xu, Y., Ahmed, S., Feng, S., Mokashi, V.P., and Chain, P.S. 2016. Enabling the democratization of the genomics revolution with a fully integrated web-based bioinformatics platform. Nucleic Acids Res. 45, 67–80.CrossRefGoogle Scholar
  28. Lim, W.J., Park, S.R., An, C.L., Lee, J.Y., Hong, S.Y., Shin, E.C., Kim, E.J., Kim, J.O., Kim, H., and Yun, H.D. 2003. Cloning and characterization of a thermostable intracellular α-amylase gene from the hyperthermophilic bacterium Thermotoga maritima MSB8. Res. Microbiol. 154, 681–687.CrossRefGoogle Scholar
  29. Liu, X.D. and Xu, Y. 2008. A novel raw starch digesting α-amylase from a newly isolated Bacillus sp. YX-1: Purification and characterization. Bioresour. Technol. 99, 4315–4320.CrossRefGoogle Scholar
  30. Makhalanyane, T.P., Van Goethem, M.W., and Cowan, D.A. 2016. Microbial diversity and functional capacity in polar soils. Curr. Opin. Biotechnol. 38, 159–166.CrossRefGoogle Scholar
  31. Manisha, and Yadav, S.K. 2017. Technological advances and applications of hydrolytic enzymes for valorization of lignocellulosic biomass. Bioresour. Technol. 245, 1727–1739.CrossRefGoogle Scholar
  32. Martins, L.O., Soares, C.M., Pereira, M.M., Teixeira, M., Costa, T., Jones, G.H., and Henriques, A.O. 2002. Molecular and biochemical characterization of a highly stable bacterial laccase that occurs as a structural component of the Bacillus subtilis endospore coat. J. Biol. Chem. 277, 18849–18859.CrossRefGoogle Scholar
  33. Mathews, S.L., Smithson, C.E., and Grunden, A.M. 2016. Purification and characterization of a recombinant laccase-like multi-copper oxidase from Paenibacillus glucanolyticus SLM1. J. Appl. Microbiol. 121, 1335–1345.CrossRefGoogle Scholar
  34. Matzke, J., Schwermann, B., and Bakker, E.P. 1997. Acidostable and acidophilic proteins: The example of the α-amylase from Alicyclobacillus acidocaldarius. Comp. Biochem. Physiol. 118, 475–479.CrossRefGoogle Scholar
  35. Maurya, D.P., Singla, A., and Negi, S. 2015. An overview of key pretreatment processes for biological conversion of lignocellulosic biomass to bioethanol. 3 Biotech. 5, 597–609.CrossRefGoogle Scholar
  36. McDonald, A.G., Boyce, S., and Tipton, K.F. 2008. ExplorEnz: The primary source of the IUBMB enzyme list. Nucleic Acids Res. 37, D593–D597.CrossRefGoogle Scholar
  37. Moghadam, M.S., Albersmeier, A., Winkler, A., Cimmino, L., Rise, K., Hohmann-Marriott, M.F., Kalinowski, J., Rückert, C., Wentzel, A., and Lale, R. 2016. Isolation and genome sequencing of four Arctic marine Psychrobacter strains exhibiting multicopper oxidase activity. BMC Genomics 17, 117.CrossRefGoogle Scholar
  38. Niederberger, T.D., McDonald, I.R., Hacker, A.L., Soo, R.M., Barrett, J.E., Wall, D.H., and Cary, S.C. 2008. Microbial community composition in soils of Northern Victoria Land, Antarctica. Environ. Microbiol. 10, 1713–1724.CrossRefGoogle Scholar
  39. Niladevi, K.N., Jacob, N., and Prema, P. 2008. Evidence for a halotolerant-alkaline laccase in Streptomyces psammoticus: Purification and characterization. Process Biochem. 43, 654–660.CrossRefGoogle Scholar
  40. Nurachman, Z., Kurniasih, S.D., Puspitawati, F., Hadi, S., Radjasa, O.K., and Natalia, D. 2010. Cloning of the endoglucanase gene from a Bacillus amyloliquefaciens PSM3.1 in Escherichia coli revealed catalytic triad residues thr-his-glu. Am. J. Biochem. Biotechnol. 6, 268–274.CrossRefGoogle Scholar
  41. O’Leary, N.A., Wright, M.W., Brister, J.R., Ciufo, S., Haddad, D., McVeigh, R., Rajput, B., Robbertse, B., Smith-White, B., and Ako-Adjei, D., et al. 2016. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44, D733–D745.CrossRefGoogle Scholar
  42. Oh, H.N., Lee, T.K., Park, J.W., No, J.H., Kim, D., and Sul, W.J. 2017. Metagenomic SMRT sequencing-based exploration of novel lignocellulose-degrading capability in wood detritus from Torreya nucifera in Bija Forest on Jeju island. J. Microbiol. Biotechnol. 27, 1670–1680.CrossRefGoogle Scholar
  43. Pedersen, M., Johansen, K.S., and Meyer, A.S. 2011. Low temperature lignocellulose pretreatment: effects and interactions of pretreatment pH are critical for maximizing enzymatic monosaccharide yields from wheat straw. Biotechnol. Biofuels 4, 11.CrossRefGoogle Scholar
  44. Pereira, J.H., Chen, Z., McAndrew, R.P., Sapra, R., Chhabra, S.R., Sale, K.L., Simmons, B.A., and Adams, P.D. 2010. Biochemical characterization and crystal structure of endoglucanase Cel5a from the hyperthermophilic Thermotoga maritima. J. Struct. Biol. 172, 372–379.CrossRefGoogle Scholar
  45. Rabemanolontsoa, H. and Saka, S. 2016. Various pretreatments of lignocellulosics. Bioresour. Technol. 199, 83–91.CrossRefGoogle Scholar
  46. Rhoads, A. and Au, K.F. 2015. PacBio sequencing and its applications. Genomics Proteomics Bioinformatics 13, 278–289.CrossRefGoogle Scholar
  47. Samie, N., Noghabi, K.A., Gharegozloo, Z., Zahiri, H.S., Ahmadian, G., Sharafi, H., Behrozi, R., and Vali, H. 2012. Psychrophilic α-amylase from Aeromonas veronii NS07 isolated from farm soils. Process Biochem. 47, 1381–1387.CrossRefGoogle Scholar
  48. Seemann, T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069.CrossRefGoogle Scholar
  49. Shafiei, M., Ziaee, A.A., and Amoozegar, M.A. 2010. Purification and biochemical characterization of a novel SDS and surfactant stable, raw starch digesting, and halophilic α-amylase from a moderately halophilic bacterium, Nesterenkonia sp. strain F. Process Biochem. 45, 694–699.CrossRefGoogle Scholar
  50. Simmons, C.W., Reddy, A.P., D’haeseleer, P., Khudyakov, J., Billis, K., Pati, A., Simmons, B.A., Singer, S.W., Thelen, M.P., and VanderGheynst, J.S. 2014. Metatranscriptomic analysis of lignocellulolytic microbial communities involved in high-solids decomposition of rice straw. Biotechnol. Biofuels 7, 495.CrossRefGoogle Scholar
  51. Struvay, C. and Feller, G. 2012. Optimization to low temperature activity in psychrophilic enzymes. Int. J. Mol. Sci. 13, 11643–11665.CrossRefGoogle Scholar
  52. Sun, Y. and Cheng, J. 2002. Hydrolysis of lignocellulosic materials for ethanol production: a review. Bioresour. Technol. 83, 1–11.CrossRefGoogle Scholar
  53. Tian, M., Du, D., Zhou, W., Zeng, X., and Cheng, G. 2017. Phenol degradation and genotypic analysis of dioxygenase genes in bacteria isolated from sediments. Braz. J. Microbiol. 48, 305–313.CrossRefGoogle Scholar
  54. Ventorino, V., Ionata, E., Birolo, L., Montella, S., Marcolongo, L., de Chiaro, A., Espresso, F., Faraco, V., and Pepe, O. 2016. Lignocellulose-adapted endo-cellulase producing streptomyces strains for bioconversion of cellulose-based materials. Front. Microbiol. 7, 2061.CrossRefGoogle Scholar
  55. Wang, C., Dong, D., Wang, H., Müller, K., Qin, Y., Wang, H., and Wu, W. 2016a. Metagenomic analysis of microbial consortia enriched from compost: new insights into the role of actinobacteria in lignocellulose decomposition. Biotechnol. Biofuels 9, 22.CrossRefGoogle Scholar
  56. Wang, L., Nie, Y., Tang, Y.Q., Song, X.M., Cao, K., Sun, L.Z., Wang, Z.J., and Wu, X.L. 2016b. Diverse bacteria with lignin degrading potentials isolated from two ranks of coal. Front. Microbiol. 7, 1428.PubMedPubMedCentralGoogle Scholar
  57. Yeager, C.M., Gallegos-Graves, V., Dunbar, J., Hesse, C.N., Daligault, H., and Kuske, C.R. 2017. Polysaccharide degradation capability of Actinomycetales soil isolates from a Semiarid Grassland of the Colorado Plateau. Appl. Environ. Microbiol. 83, pii: e03020-16.Google Scholar
  58. Yin, Y., Mao, X., Yang, J., Chen, X., Mao, F., and Xu, Y. 2012. Dbcan: A web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 40, W445–W451.CrossRefGoogle Scholar
  59. Yu, N.H., Kim, J.A., Jeong, M.H., Cheong, Y.H., Hong, S.G., Jung, J.S., Koh, Y.J., and Hur, J.S. 2014. Diversity of endophytic fungi associated with bryophyte in the maritime Antarctic (King George Island). Polar Biol. 37, 27–36.CrossRefGoogle Scholar

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© The Microbiological Society of Korea 2019

Authors and Affiliations

  1. 1.Department of Systems BiotechnologyChung-Ang UniversityAnseongRepublic of Korea
  2. 2.Division of Polar Life SciencesKorea Polar Research InstituteIncheonRepublic of Korea

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