Biodiversity of Plant Polysaccharide-Degrading Bacteria in Mangrove Ecosystem
Main Article Content
Abstract
The mangrove ecosystem is the most productive environment and represent a rich biological diversity including microorganisms. Plant polysaccharides, such as cellulose, hemicellulose and pectin are significant carbon sources of the ecosystem. Bacteria play an important role in carbon cycle in the ecosystem as a decomposer. Based on culture-dependent methods, many plant polysaccharide-degrading bacteria were isolated from mangrove sediments. However, only four bacterial phyla were found in the isolates. In contrast, functional and taxonomic analysis of metagenomic datasets indicated that 10 to 12 bacterial phyla involve in hemicellulose degradation. A large number of anaerobic bacteria, such as the genera Clostridum, Dictyoglomus Marinitoga, Petrotoga, Thermotoga and Verrucomicrobia, were found among them. In addition, many hemicellulose degradation enzymes were found in the phylum Acidobacteria which are abundant and ubiquitous across soil environments. These results suggest that various kinds of bacteria including anaerobic bacteria contribute Plant polysaccharide degradation.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
References
Ademark P, Varga A, Medve J, Harjunpää V, Drakenberg T, Tjerneld F and Stålbrand H. (1998). Softwood hemicellulose-degrading enzymes from Aspergillus niger: Purification and properties of a ?-mannanase. Journal of Biotechnology 63(3): 199–210. https://doi.org/10.1016/S0168-1656(98)00086-8
Aksornkoae S. (1986). Mangrove ecosystem general background. In: Training course on life history of selected species of flora and fauna in mangrove ecosystems. UNDP/ UNESCO Regional Project (RAS/86/120), 17–23.
Alzubaidy H, Essack M, Malas T B, Bokhari A, Motwalli O, Kamanu F K, Jamhor S A, et al. (2016). Rhizosphere microbiome metagenomics of gray mangroves (Avicennia marina) in the Red Sea. Gene 576(2): 626–636. https://doi.org/10.1016/j.gene.2015.10.032
Amann R I, Ludwig W and Schleifer K H. (1995). Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiology and Molecular Biology Review 59(1): 143–169.
Arijit D, Sourav B, Reddy N and Rajan S. (2013). Improved production and purification of pectinase from Streptomyces sp. GHBA10 isolated from Valapattanam mangrove habitat, Kerala, India. International Research Journal of Biological Sciences 2(3): 16–22.
Baba A, Miyazaki M, Nagahama T and Nogi Y. (2011). Microbulbifer chitinilyticus sp. nov. and Microbulbifer okinawensis sp. nov., chitin-degrading bacteria isolated from mangrove forests. International Journal of Systematic and Evolutionary Microbiology 61(9): 2215–2220. https://doi.org/10.1099/ijs.0.024158-0
Behera B, Parida S, Dutta S and Thatoi H. (2014). Isolation and identification of cellulose degrading bacteria from mangrove soil of Mahanadi River Delta and their cellulase production ability. American Journal of Microbiological Research 2(1): 41–46. https://doi.org/10.12691/ajmr-2-1-6
Behera B, Sethi B, Mishra R, Dutta S and Thatoi H. (2017). Microbial cellulases–Diversity & biotechnology with reference to mangrove environment: A review. Journal of Genetic Engineering and Biotechnology 15(1): 197–210. https://doi.org/10.1016/j.jgeb.2016.12.001
Bibi F, Ullah I, Alvi S, Bakhsh S, Yasir M, Al-Ghamdi A and Azhar E. (2017). Isolation, diversity, and biotechnological potential of rhizo-and endophytic bacteria associated with mangrove plants from Saudi Arabia. Genetics and Molecular Research, 16(2): 1–12. https://doi.org/10.4238/gmr16029657
Biely P, Singh S and Puchart V. (2016). Towards enzymatic breakdown of complex plant xylan structures: State of the art. Biotechnology Advances 34: 1260–1274. https://doi.org/10.1016/j.biotechadv.2016.09.001
Blouzard J C, Coutinho P M, Fierobe H P, Henrissat B, Lignon S, Tardif C, Pagès S and de Philip P. (2010). Modulation of cellulosome composition in Clostridium cellulolyticum: Adaptation to the polysaccharide environment revealed by proteomic and carbohydrate-active enzyme-analyses. Proteomics 10(3): 541–554. https://doi.org/10.1002/pmic.200900311
Bray J R and Gorham E. (1964). Litter production in forests of the world. In: J B Cragg (ed.). Advances in ecological research (Volume 2). London and New York: Academic Press, 101–157. https://doi.org/10.1016/S0065-2504(08)60331-1
Brumm P J, Gowda K, Robb F T and Mead D A. (2016). The complete genome sequence of hyperthermophile Dictyoglomus turgidum DSM 6724™ reveals a specialized carbohydrate fermentor. Frontiers in Microbiology 7: 1979. https://doi.org/10.3389/fmicb.2016.01979
Bunt J, Boto K and Boto G. (1979). A survey method for estimating potential levels of mangrove forest primary production. Marine Biology 52(2): 123–128. https://doi.org/10.1007/BF00390419
Castro R A, Quecine M C, Lacava P T, Batista B D, Luvizotto D M, Marcon J and Ferreira A, et al. (2014). Isolation and enzyme bioprospection of endophytic bacteria associated with plants of Brazilian mangrove ecosystem. SpringerPlus 3(1): 382. https://doi.org/10.1186/2193-1801-3-382
Collins T, Gerday C and Feller G. (2005). Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiology Reviews 29(1): 3–23. https://doi.org/10.1016/j.femsre.2004.06.005
Collmer A and Bateman D F. (1981). Impaired induction and self-catabolite repression of extracellular pectate lyase in Erwinia chrysanthemi mutants deficient in oligogalacturonide lyase. Proceedings of the National Academy of Sciences 78(6): 3920–3924. https://doi.org/10.1073/pnas.78.6.3920
Contesini F, Liberato M V, Rubio M V, Calzado F, Zubieta M P, Riaño-Pachón D M, Squina F M, Bracht F, Skaf M S and Damasio A R. (2017). Structural and functional characterization of a highly secreted ?-L-arabinofuranosidase (GH62) from Aspergillus nidulans grown on sugarcane bagasse. BBA – Proteins and Proteomics 1865(12): 1758–1769. https://doi.org/10.1016/j.bbapap.2017.09.001
Dekker R F and Richards G N. (1976). Hemicellulases: Their occurrence, purification, properties, and mode of action. In: R S Tipson and D Horton (eds.). Advances in Carbohydrate Chemistry and Biochemistry (Volume 32). New York, San Francisco and London: Academic Press, 277–352. https://doi.org/10.1016/S0065-2318(08)60339-X
Dinesh B, Furusawa G and Amirul A A A. (2017). Mangrovimonas xylaniphaga sp. nov. isolated from estuarine mangrove sediment of Matang Mangrove Forest, Malaysia. Archives of Microbiology 199(1): 63–67. https://doi.org/10.1007/s00203-016-1275-8
Dinesh B, Lau N -S, Furusawa G, Kim S -W, Taylor T D, Foong S Y and Shu-Chien A C. (2016). Comparative genome analyses of novel Mangrovimonas-like strains isolated from estuarine mangrove sediments reveal xylan and arabinan utilization genes. Marine Genomics 25: 115–121. https://doi.org/10.1016/j.margen.2015.12.006
Dubey A K, Yadav S, Kumar M, Anand G and Yadav D. (2016). Molecular biology of microbial pectate lyase: A review. British Biotechnology Journal 13(1): 1–26. https://doi.org/10.9734/BBJ/2016/24893
Felix C R and Ljungdahl L G. (1993). The cellulosome: The exocellular organelle of Clostridium. Annual Review of Microbiology 47(1): 791–819. https://doi.org/10.1146/annurev.mi.47.100193.004043
Gal L, Pages S, Gaudin C, Belaich A, Reverbel-Leroy C, Tardif C and Belaich J-P. (1997). Characterization of the cellulolytic complex (cellulosome) produced by Clostridium cellulolyticum. Applied and Environmental Mirobiology 63(3): 903–990.
Gao Z-M, Xiao J, Wang X-N, Ruan L-W, Chen X-L and Zhang Y-Z. (2012). Vibrio xiamenensis sp. nov., a cellulase-producing bacterium isolated from mangrove soil. International Journal of Systematic and Evolutionary Microbiology 62(8): 1958–1962. https://doi.org/10.1099/ijs.0.033597-0
Gibbs M D, Reeves R A and Bergquist P L. (1995). Cloning, sequencing, and expression of a xylanase gene from the extreme thermophile Dictyoglomus thermophilum Rt46B. 1 and activity of the enzyme on fiber-bound substrate. Applied and Environmental Microbiology 61(12): 4403–4408.
Haldar S and Nazareth S W. (2018). Taxonomic diversity of bacteria from mangrove sediments of Goa: Metagenomic and functional analysis. 3 Biotech 8(10): 436. https://doi.org/10.1007/s13205-018-1441-6
Harholt J, Suttangkakul A and Scheller H V. (2010). Biosynthesis of pectin. Plant Physiology 153(2): 384–395. https://doi.org/10.1104/pp.110.156588
Holguin G, Vazquez P and Bashan Y. (2001). The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: An overview. Biology and Fertility of Soils 33(4): 265–278. https://doi.org/10.1007/s003740000319
Imchen M, Kumavath R, Barh D, Azevedo V, Ghosh P, Viana M and Wattam A R. (2017). Searching for signatures across microbial communities: Metagenomic analysis of soil samples from mangrove and other ecosystems. Scientific Reports 7(1): 8859. https://doi.org/10.1038/s41598-017-09254-6
Imran M, Pant P, Shanbhag Y P, Sawant S V and Ghadi S C. (2017). Genome sequence of Microbulbifer mangrovi DD-13 T reveals its versatility to degrade multiple polysaccharides. Marine Biotechnology 19(1): 116–124. https://doi.org/10.1007/s10126-017-9737-9
Kalaiselvi V, Jayalakshmi, S and Narayanan R. (2013). Biofuel production using marine microbes. International Journal of Current Microbiology and Applied Sciences 2(5): 67–74.
Kathiresan K and Bingham B L. (2001). Biology of mangroves and mangrove ecosystems. Advances in Marine Biology 40: 81–251. https://doi.org/10.1016/S0065-2881(01)40003-4
Katsimpouras C, Dimarogona M, Petropoulos P, Christakopoulos P and Topakas E. (2016). A thermostable GH26 endo-?-mannanase from Myceliophthora thermophila capable of enhancing lignocellulose degradation. Applied Microbiology and Biotechnology 100(19): 8385–8397. https://doi.org/10.1007/s00253-016-7609-2
Keegstra K. (2010). Plant cell walls. Plant Physiology 154(2): 483–486. https://doi.org/10.1104/pp.110.161240
Khandeparker R, Verma P and Deobagkar D. (2011). A novel halotolerant xylanase from marine isolate Bacillus subtilis cho40: Gene cloning and sequencing. New Biotechnology 28(6): 814–821. https://doi.org/10.1016/j.nbt.2011.08.001
Kosugi A, Murashima K and Doi R H. (2002). Xylanase and acetyl xylan esterase activities of XynA, a key subunit of the Clostridium cellulovorans cellulosome for xylan degradation. Applied and Environmental Microbiology 68(12): 6399–6402. https://doi.org/10.1128/AEM.68.12.6399-6402.2002
Lang C and Dörnenburg H. (2000). Perspectives in the biological function and the technological application of polygalacturonases. Applied Microbiology and Biotechnology 53(4): 366–375. https://doi.org/10.1007/s002530051628
Law J W-F, Ser H-L, Ab Mutalib N -S, Saokaew S, Duangjai A, Khan T M, Chan K-G, Goh B-H and Lee L-H. (2019). Streptomyces monashensis sp. nov., a novel mangrove soil actinobacterium from East Malaysia with antioxidative potential. Scientific Reports 9(1): 3056. https://doi.org/10.1038/s41598-019-39592-6
Lee L-H, Azman A-S, Zainal N, Eng S-K, Ab Mutalib N-S, Yin W-F and Chan K-G. (2014a). Microbacterium mangrovi sp. nov., an amylolytic actinobacterium isolated from mangrove forest soil. International Journal of Systematic and Evolutionary Microbiology 64(10): 3513–3519. https://doi.org/10.1099/ijs.0.062414-0
Lee L-H, Azman A-S, Zainal N, Eng S-K, Fang C-M, Hong K and Chan K-G. (2014b). Novosphingobium malaysiense sp. nov. isolated from mangrove sediment. International Journal of Systematic and Evolutionary Microbiology 64(4): 1194–1201. https://doi.org/10.1099/ijs.0.062414-0
Li G, Jiang Y, Fan X-J and Liu Y-H. (2012). Molecular cloning and characterization of a novel ?-glucosidase with high hydrolyzing ability for soybean isoflavone glycosides and glucose-tolerance from soil metagenomic library. Bioresource Technology 123: 15–22. https://doi.org/10.1016/j.biortech.2012.07.083
Liao J, Okuyama M, Ishihara K, Yamori Y, Iki S, Tagami T, Mori H, Chiba S and Kimura A. (2016). Kinetic properties and substrate inhibition of ?-galactosidase from Aspergillus niger. Bioscience, Biotechnology, and Biochemistry 80(9): 1747–1752. https://doi.org/10.1080/09168451.2015.1136884
Lyimo T J, Pol A, Harhangi H R, Jetten M S and Op den Camp H J. (2009). Anaerobic oxidation of dimethylsulfide and methanethiol in mangrove sediments is dominated by sulfate-reducing bacteria. FEMS Microbiology Ecology 70(3): 483–492. https://doi.org/10.1111/j.1574-6941.2009.00765.x
Mai Z, Su H, Yang J, Huang S and Zhang S. (2014). Cloning and characterization of a novel GH44 family endoglucanase from mangrove soil metagenomic library. Biotechnology Letters 36(8): 1701–1709. https://doi.org/10.1007/s10529-014-1531-4
Mayans O, Scott M, Connerton I, Gravesen T, Benen J, Visser J, Pickersgill R and Jenkins J. (1997). Two crystal structures of pectin lyase A from Aspergillus reveal a pH driven conformational change and striking divergence in the substrate-binding clefts of pectin and pectate lyases. Structure 5(5): 677–689. https://doi.org/10.1016/S0969-2126(97)00222-0
Mendes L W and Tsai S M. (2018). Distinct taxonomic and functional composition of soil microbiomes along the gradient forest-restinga-mangrove in southeastern Brazil. Antonie van Leeuwenhoek 111(1): 101–114. https://doi.org/10.1007/s10482-017-0931-6
Mohand-Oussaid O, Payot S, Guedon E, Gelhaye E, Youyou A and Petitdemange H. (1999). The extracellular xylan degradative system in Clostridium cellulolyticum cultivated on Xylan: Evidence for cell-free cellulosome production. Journal of Bacteriology 181(13): 4035–4040.
Naresh S, Kunasundari B, Gunny A A N, Teoh Y P, Shuit S H, Ng Q H and Hoo P Y. (2019). Isolation and partial characterisation of thermophilic cellulolytic bacteria from North Malaysian tropical mangrove soil. Tropical Life Sciences Research 30(1): 123–147. https://doi.org/10.21315/tlsr2019.30.1.8
Nasuno S and Starr M P. (1966). Polygalacturonase of Erwinia carotovora. Journal of Biological Chemistry 241(22): 5298–5306.
Omar S M, Farouk N M, Malek N A and Abidin Z A Z. (2017). Verrucosispora sp. K2- 04, potential xylanase producer from Kuantan Mangrove Forest Sediment. International Journal of Food Engineering 3(2): 165–168. https://doi.org/10.18178/ijfe.3.2.165-168
Ottoni J R, Cabral L, de Sousa S T P, Lacerda Júnior G V, Domingos D F, Soares Junior F L, da Silva M C P, Marcon J, Franco Dias A C, de Melo I S, de Souza A P, Andreote F D and de Oliveira V M. (2017). Functional metagenomics of oil-impacted mangrove sediments reveals high abundance of hydrolases of biotechnological interest. World Journal of Microbiology and Biotechnology 33(7): 141. https://doi.org/10.1007/s11274-017-2307-5
Pandey S, Singh S, Yadav A N, Nain L and Saxena A K. (2013). Phylogenetic diversity and characterization of novel and efficient cellulase producing bacterial isolates from various extreme environments. Bioscience, Biotechnology, and Biochemistry 77(7): 1474–1480. https://doi.org/10.1271/bbb.130121
Pettolino F A, Walsh C, Fincher G B and Bacic A. (2012). Determining the polysaccharide composition of plant cell walls. Nature Protocols 7(9): 1590–1607. https://doi.org/10.1038/nprot.2012.081
Polidoro B A, Carpenter K E, Collins L, Duke N C, Ellison A M, Ellison J C, Farnsworth E J, et al. (2010). The loss of species: mangrove extinction risk and geographic areas of global concern. PloS one 5(4): e10095. https://doi.org/10.1371/journal.pone.0010095
Prade R A, Zhan D, Ayoubi P and Mort A J. (1999). Pectins, pectinases and plant-microbe interactions. Biotechnology and Genetic Engineering Reviews 16(1): 361–392. https://doi.org/10.1080/02648725.1999.10647984
Priya G, Lau N -S, Furusawa G, Dinesh B, Foong S Y and Amirul A A A. (2018). Metagenomic insights into the phylogenetic and functional profiles of soil microbiome from a managed mangrove in Malaysia. Agri Gene 9: 5–15. https://doi.org/10.1016/j.aggene.2018.07.001
Sabathé F, Bélaïch A and Soucaille P. (2002). Characterization of the cellulolytic complex (cellulosome) of Clostridium acetobutylicum. FEMS Microbiology Letters 217(1): 15–22. https://doi.org/10.1111/j.1574-6968.2002.tb11450.x
Sakai K, Kojiya S, Kamijo J, Tanaka K, Maebayashi M, Oh J-S, Ito M, Hori M, Shimizu M and Kato M. (2017). Oxygen-radical pretreatment promotes cellulose degradation by cellulolytic enzymes. Biotechnology for Biofuels 10: 290. https://doi.org/10.1186/s13068-017-0979-6
Scheller H V and Ulvskov P. (2010). Hemicelluloses. Annual Review of Plant Biology 61: 263–289. https://doi.org/10.1146/annurev-arplant-042809-112315
Shallom D and Shoham Y. (2003). Microbial hemicellulases. Current Opinion in Microbiology 6(3): 219–228. https://doi.org/10.1016/S1369-5274(03)00056-0
Siew C K, Williams P A and Young N W. (2005). New insights into the mechanism of gelation of alginate and pectin: Charge annihilation and reversal mechanism. Biomacromolecules 6(2): 963–969. https://doi.org/10.1021/bm049341l
Soares Júnior F L, Dias A C F, Fasanella C C, Taketani R G, de Souza Lima A O, Melo I S and Andreote F D. (2013). Endo-and exoglucanase activities in bacteria from mangrove sediment. Brazilian Journal of Microbiology 44(3): 969–976. https://doi.org/10.1590/S1517-83822013000300048
Soccol C R, da Costa E S F, Letti L A J, Karp S G, Woiciechowski A L and de Souza Vandenberghe L P. (2017). Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation 1: 52–71. https://doi.org/10.1016/j.biori.2017.01.002
Somerville C. (2006). Cellulose synthesis in higher plants. Annual Reviews of Cell and Developmental Biology 22: 53–78. https://doi.org/10.1146/annurev.cellbio.22.022206.160206
Tabao N S C and Monsalud R G. (2010). Characterization and identification of high cellulaseproducing bacterial strains from Philippine mangroves. Philippine Journal of Systematic Biology 4: 13–20. https://doi.org/10.3860/pjsb.v4i0.1562
Taketani R G. Franco N O, Rosado A S and van Elsas J D. (2010). Microbial community response to a simulated hydrocarbon spill in mangrove sediments. The Journal of Microbiology 48(1): 7–15. https://doi.org/10.1007/s12275-009-0147-1
Thatoi H, Behera B, Dangar T and Mishra R. (2012). Microbial biodiversity in mangrove soil of Bhitarakanika, Odisha, India. International Journal of Environmental Biology 2(2): 50–58.
Thatoi H, Behera B C, Mishra R R and Dutta S K. (2013). Biodiversity and biotechnological potential of microorganisms from mangrove ecosystems: A review. Annals of Microbiology 63(1): 1–19. https://doi.org/10.1007/s13213-012-0442-7
Thomas L, Sindhu R and Pandey A. (2013). Identification and characterization of a highly alkaline and thermotolerant novel xylanase from Streptomyces sp. Biologia 68(6): 1022–1027. https://doi.org/10.2478/s11756-013-0248-5
Thompson C E, Beys-da-Silva W O, Santi L, Berger M, Vainstein M H and Vasconcelos A T R. (2013). A potential source for cellulolytic enzyme discovery and environmental aspects revealed through metagenomics of Brazilian mangroves. AMB Express 3(1): 65. https://doi.org/10.1186/2191-0855-3-65
Vashist P, Nogi Y, Ghadi S C, Verma P and Shouche Y S. (2013). Microbulbifer mangrovi sp. nov., a polysaccharide-degrading bacterium isolated from an Indian mangrove. International Journal of Systematic and Evolutionary Microbiology 63: 2532–2537. https://doi.org/10.1099/ijs.0.042978-0
Wang G, Meng K, Luo H, Wang Y, Huang H, Shi P, Yang P, Zhang Z and Yao B. (2012). Phylogenetic diversity and environment-specific distributions of glycosyl hydrolase family 10 xylanases in geographically distant soils. PloS one 7(8); e43480. https://doi.org/10.1371/journal.pone.0043480
Wang J, Zhang Y, Qin X, Gao L, Han B, Zhang D, Li J, Huang H and Zhang W. (2017). Efficient expression of an acidic endo-polygalacturonase from Aspergillus niger and its application in juice production. Journal of Agricultural and Food Chemistry 65(13): 2730–2736. https://doi.org/10.1021/acs.jafc.6b05109
Wang L, Shi H, Xu B, Li X, Zhang Y and Wang F. (2016). Characterization of Thermotoga thermarum DSM 5069 ?-glucuronidase and synergistic degradation of xylan. BioResources 11(3): 5767–5779. https://doi.org/10.15376/biores.11.3.5767-5779
Ward N L, Challacombe J F, Janssen P H, Henrissat B, Coutinho P M, Wu M, Xie G, et al. (2009). Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Applied Environmental Microbiology 75(7): 2046–2056. https://doi.org/10.1128/AEM.02294-08
Xie Q-Y, Lin H-P, Li L, Brown R, Goodfellow M, Deng Z and Hong K. (2012). Verrucosispora wenchangensis sp. nov., isolated from mangrove soil. Antonie van Leeuwenhoek 102(1): 1–7. https://doi.org/10.1007/s10482-012-9707-1