Screening and Phylogenetic Analysis of Deep-Sea Bacteria Capable of Metabolizing Lignin-Derived Aromatic Compounds

Y. Ohta, S. Nishi, T. Haga, T. Tsubouchi, R. Hasegawa, M. Konishi, Y. Nagano, Y. Tsuruwaka, Y. Shimane, K. Mori, K. Usui, E. Suda, K. Tsutsui, A. Nishimoto, Y. Fujiwara, T. Maruyama, Y. Hatada

Institute of Biogeosciences, Japan Agency of Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan.

DOI: 10.4236/ojms.2012.24021                

Abstract

Lignin is one of the most abundant biomasses in nature. It is composed of aromatic moieties and has great potential for use in the production of chemical alternatives to petroleum products. Because of increasing interest in biocatalysis, the potential for industrial application of microbial metabolism of lignin-derived compounds has gained considerable recent attention. Functional screenings of culturable bacteria isolated from sediments and sunken wood collected from the deep sea revealed the existence of a number of previously unidentified bacteria capable of metabolizing lignin-related aromatic compounds. Of the 510 isolates obtained in the present study, 208 completely or partially metabolized these compounds. The 208 isolates were classified into diverse phyla, including Firmicutes, Actinobacteria, Bacteroidetes, and Proteobacteria. Among the 208 isolates, 61 unique 16S rRNA gene sequences were detected including previously unidentified marine lineage isolates. The metabolites of the isolates were analysed using liquid chromatography/mass spectrometry (LC/MS) or gas chromatography/mass spectrometry (GC/MS). Most of the representative 61 isolates non-oxidatively decarboxylated the substrates to produce the corresponding aromatic vinyl monomers, which are used as feed stocks for bio-based plastics production. Oxidative metabolism of the lignin-related compounds for assimilation was frequently observed. Our study showed that the deep-sea environment contains an abundance of microorganisms capable of both non-oxidative and oxidative bioconversion of lignin-derived aromatic compounds. The ability for bio-conversion of aromatic compounds found in this study will facilitate the development of future biotechnological applications.

Keywords

Aromatic Compound; Bacteria; Deep Sea; Lignin

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	T. K. Kirk and R. L. Farrell, “Enzymatic Combustion— The Microbial-Degradation of Lignin,” Annual Review of Microbiology, Vol. 41, No. 1, 1987, pp. 465-505. doi:10.1146/annurev.mi.41.100187.002341
[2]	M. N. S. Kumar, A. K. Mohanty, L. Erickson and M. Misra, “Lignin and Its Applications with Polymers,” Journal of Biobased Materials and Bioenergy, Vol. 3, No. 1, 2009, pp. 1-24. doi:10.1166/jbmb.2009.1001
[3]	D. Stewart, “Lignin as a Base Material for Materials Applications: Chemistry, Application and Economics,” Industrial Crops and Products, Vol. 27, No. 2, 2008, pp. 202-207.
[4]	F. G. Calvo-Flores and J. A. Dobado, “Lignin as Renewable Raw Material,” Chemsuschem, Vol. 3, No. 11, 2010, pp. 1227-1235. doi:10.1002/cssc.201000157
[5]	J. Du, Z. Y. Shao and H. M. Zhao, “Engineering Microbial Factories for Synthesis of Value-added Products,” Journal of Industrial Microbiology & Biotechnology, Vol. 38, No. 10, 2011, pp. 873-890. doi:10.1002/cssc.201000157
[6]	M. H. Gold and M. Alic, “Molecular-Biology of the Lignin-Degrading Basidiomycete Phanerochaete chrysosporium,” Microbiological Reviews, Vol. 57, No. 3, 1993, pp. 605-622.
[7]	P. Kersten and D. Cullen, “Extracellular Oxidative Systems of the Lignin-Degrading Basidiomycete Phanerochaete chrysosporium,” Fungal Genetics and Biology, Vol. 44, No. 2, 2007, pp. 77-87. doi:10.1002/cssc.201000157
[8]	D. Martinez, L. F. Larrondo, N. Putnam, M. D. S. Gelpke, K. Huang, J. Chapman, K. G. Helfenbein, et al., “Genome Sequence of the Lignocellulose Degrading Fungus Phanerochaete chrysosporium strain RP78,” Nature Biotechnology, Vol. 22, No. 6, 2004, pp. 695-700. doi:10.1038/nbt967
[9]	D. Martinez, J. Challacombe, I. Morgenstern, D. Hibbett, M. Schmoll, C. P. Kubicek, et al., “Genome, Transcriptome, and Secretome Analysis of Wood Decay Fungus Postia Placenta Supports Unique Ｍechanisms of Ligno-cellulose Conversion,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 106, No. 6, 2009, pp. 1954-1959.
[10]	D. L. Crawford, A. L. Pometto and R. L. Crawford, “Lignin Degradation by Streptomyces viridosporus—Isolation and Characterization of a New Polymeric Lignin Degra-dation Intermediate,” Applied and Environmental Micro-biology, Vol. 45, No. 3, 1983, pp. 898-904.
[11]	J. Trojanowski, K. Haider and V. Sundman, “Decomposition of C-14-Labeled Lignin and Phenols by a Nocardia sp.,” Archives of Microbiology, Vol. 114, No. 2, 1977, pp. 149-153. doi:10.1007/BF00410776
[12]	E. Masai, Y. Katayama and M. Fukuda, “Genetic and Biochemical Investigations on Bacterial Catabolic Pathways for Lignin-Derived Aromatic Compounds,” Bioscience Biotechnology and Biochemistry, Vol. 71, No. 1, 2007, pp. 1-15. doi:10.1271/bbb.60437
[13]	M. Ahmad, C. R. Taylor, D. Pink, K. Burton, D. East- wood, G. D. Bending and T. D. H. Bugg, “Development of Novel Assays for Lignin Degradation: Comparative Analysis of Bacterial and Fungal Lignin Degraders,” Molecular Biosystems, Vol. 6, No. 5, 2010, pp. 815-821. doi:10.1039/b908966g
[14]	T. D. H. Bugg, M. Ahmad, E. M. Hardiman and R. Singh, “The Emerging Role for Bacteria in Lignin Degradation and Bio-product Formation,” Current Opinion in Bio-technology, Vol. 22, No. 3, 2011, pp. 394-400. doi:10.1016/j.copbio.2010.10.009
[15]	E. B. Garethjones, R. D. Turner, S. E. J. Furtado and H. Kuhne, “Marine Biodeteriogenic Organisms. 1. Ligni-colous Fungi and Bacteria and Wood Boring Mollusca and Crustacea,” International Biodeterioration Bulletin, Vol. 12, No. 4, 1976, pp. 120-134.
[16]	M. Pailleret, T. Haga, P. Petit, C. Prive-Gill, N. Saedlou, F. Gaill and M. Zbinden, “Sunken Wood from the Vanuatu Islands: Identification of Wood Substrates and Preliminary Description of Associated Fauna,” Marine Ecology—An Evolutionary Perspective, Vol. 28, No. 1, 2007, pp. 233-241.
[17]	S. Rohrmann and H. P. Molitoris, “Screening for Wood-Degrading Enzymes in Marine Fungi,” Canadian Journal of Botany-Revue Canadienne de Botanique, Vol. 70, No. 10, 1992, pp. 2116-2123. doi:10.1139/b92-263
[18]	W. Appeltans, P. Bouchet, G. A. Boxshall, C. De Broyer, N. J. de Voogd, D. P. Gordon, B. W. Hoeksema, T. Horton, M. Kennedy, J. Mees, G. C. B. Poore, G. Read, S. St?hr, T. C. Walter and M. J. Costello, “World Register of Marine Species,” 2012. http://www.marinespecies.org
[19]	I. Wagner-Dobler and H. Biebl, “Environmental Biology of the Marine Roseobacter lineage,” Annual Review of Microbiology, Annual Reviews, Vol. 60, 2006, 2006, pp. 255-280.
[20]	M. A. Moran, R. Belas, M. A. Schell, J. M. Gonzalez, F. Sun, S. Sun, B. J. Binder, A. Buchan, et al., “Ecological Genomics of Marine Roseobacters,” Applied and Environmental Microbiology, Vol. 73, No. 14, 2007, pp. 4559- 4569. doi:10.1128/AEM.02580-06
[21]	O. Pinyakong, H. Habe and T. Omori, “The Unique Aromatic Catabolic Genes in Sphingomonads Degrading Polycyclic Aromatic Hydrocarbons (PAHs),” Journal of General and Applied Microbiology, Vol. 49, No. 1, 2003, pp. 1-19. doi:10.2323/jgam.49.1
[22]	M. T. Garcia, A. Ventosa and E. Mellado, “Catabolic Versatility of Aromatic Compound-degrading Halophilic Bacteria,” FEMS Microbiology Ecology, Vol. 54, No. 1, 2005, pp. 97-109. doi:10.1016/j.femsec.2005.03.009
[23]	H. Rodriguez, J. Landete, J. Curiel, B. Rivas, J. Mancheno and R. Munoz, “Characterization of the p-Coumaric Acid Decarboxylase from Lactobacillus plantarum CECT 748T,” Journal of Agricultural and Food Chemistry, Vol. 56, No. 9, 2008, pp. 3068-3072.
[24]	J. F. Heidelberg, I. T. Paulsen, K. E. Nelson, E. J. Gaidos, W. C. Nelson, T. D. Read, et al., “Genome Sequence of the Dissimilatory Metal Ion-Reducing Bacterium She-wanella oneidensis,” Nature Biotechnology, Vol. 20, No. 11, 2002, pp. 1118-1123. doi:10.1038/nbt749
[25]	C. S. Harwood and R. E. Parales, “The Ketoadipate Path-way and the Biology of Self-Identity,” Annual Review of Microbiology, Vol. 50, 1996, pp. 553-590. doi:10.1146/annurev.micro.50.1.553
[26]	E. Masai, M. Sasaki, Y. Minakawa, T. Abe, T. Sonoki, K. Miyauchi, Y. Katayama and M. Fukuda, “A Novel Tetrahydrofolate-Dependent O-Demethylase Gene Is Essential for Growth of Sphingomonas paucimobilis SYK-6 with Syringate,” Journal of Bacteriology, Vol. 186, No. 9, 2004, pp. 2757-2765. doi:10.1128/JB.186.9.2757-2765.2004
[27]	J. M. Gonzalez, W. B. Whitman, R. E. Hodson and M. A. Moran, “Identifying Numerically Abundant Culturable Bcteria from Complex Communities: An Example from a Lignin Enrichment Culture,” Applied and Environmental Microbiology, Vol. 62, No. 12, 1996, pp. 4433-4440.
[28]	B. Y. Tian, Q. G. Huang, Y. Xu, C. X. Wang, R. R. Lv and J. Z. Huang, “Microbial Community Structure and Diversity in a Native Forest Wood-Decomposed Hollow-Stump Ecosystem,” World Journal of Microbiology & Biotechnology, Vol. 26, No. 2, 2010, pp. 233-240. doi:10.1007/s11274-009-0165-5
[29]	V. Valaskova, W. de Boer, P. Gunnewiek, M. Pospisek and P. Baldrian, “Phylogenetic Composition and Properties of Bacteria Coexisting with the Fungus Hypholoma fasciculare in Decaying Wood,” ISME Journal, Vol. 3, No. 10, 2009, pp. 1218-1221. doi:10.1038/ismej.2009.64
[30]	S. Samadi, L. Corbari, J. Lorion, S. Hourdez, T. Haga, J. Dupont, M.-C. Boisselier and B. R. de Forges, “Biodiversity of Deep-Sea Organisms Associated with Sunken-Wood or Other Organic Remains Sampled in the Tropical Indo-Pacific,” Cahiers de Biologie Marine, Vol. 51, No. 4, 2010, pp. 459-466.
[31]	J. P. N. Rosazza, Z. Huang, L. Dostal, T. Volm and B. Rousseau, “Review: Biocatalytic Transformations of Ferulic Acid: An Abundant Aromatic Natural Product,” Journal of Industrial Microbiology, Vol. 15, No. 6. 1995, pp. 457-471. doi:10.1007/BF01570016
[32]	Z. X. Huang, L. Dostal and J. P. N. Rosazza, “Purification and Characterization of a Ferulic Acid Decarboxylase from Pseudomonas fluorescens,” Journal of Bacteriology, Vol. 176, No. 19, 1994, pp. 5912-5918.
[33]	G. Degrassi, P. P. Delaureto and C. V. Bruschi, “Purification and Characterization of Ferulate and p-Coumarate Decarboxylase from Bacillus pumilus,” Applied and Environmental Microbiology, Vol. 61, No. 1, 1995, pp. 326-332.
[34]	J. M. Salgado, R. Rodríguez-Solana, J. A. Curiel, B. de L. Rivas, R. Mu?oz, J. M. Domínguez, “Production of Vinyl Derivatives from Alkaline Hydrolysates of Corn Cobs by Recombinant Escherichia coli Containing the Phenolic Acid Decarboxylase from Lactobacillus plantarum CECT 748T,” Bioresource Technology, Vol. 117, 2012, pp. 274- 285. doi:10.1016/j.biortech.2012.04.051
[35]	S. Mathew and T. E. Abraham, “Bioconversions of Ferulic Acid, an Hydroxycinnamic Acid,” Critical Reviews in Microbiology, Vol. 32, No. 3, 2006, pp. 115-125. doi:10.1080/10408410600709628
[36]	S. Fetzner, “Ring-Cleaving Dioxygenases with a Cupin Fold,” Applied and Environmental Microbiology, Vol. 78, No. 8, 2012, pp. 2505-2514. doi:10.1128/AEM.07651-11
[37]	A. Buchan, E. L. Neidle and M. A. Moran, “Diversity of the Ring-Cleaving Dioxygenase Gene pcaH in a Salt Marsh Bacterial Community,” Applied and Environmental Microbiology, Vol. 67, No. 12, 2001, pp. 5801- 5809. doi:10.1128/AEM.67.12.5801-5809.2001
[38]	Y. Wang, J. K. Yang, O. O. Lee, S. Dash, S. C. K. Lau, A. Al-Suwailem, T. Y. H. Wong, A. Danchin and P. Y. Qian, “Hydrothermally Generated Aromatic Compounds Are Consumed by Bacteria Colonizing in Atlantis II Deep of the Red Sea,” ISME Journal, Vol. 5, No. 10, 2011, pp. 1652-1659. doi:10.1038/ismej.2011.42