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Carbohydrate metabolism genes dominant in a subtropical marine mangrove ecosystem revealed by metagenomics analysis

  • Microbial Ecology and Environmental Microbiology
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Abstract

Mangrove sediment microorganisms play a vital role in the energy transformation and element cycling in marine wetland ecosystems. Using metagenomics analysis strategy, we compared the taxonomic structure and gene profile of the mangrove and non-mangrove sediment samples at the subtropical estuary in Beibu Gulf, South China Sea. Proteobacteria, Bacteroidetes, and Firmicutes were the most abundant bacterial phyla. Archaeal family Methanosarcinaceae and bacterial genera Vibrio and Dehalococcoides were significantly higher in the mangrove sediments than in the nonmangrove sediments. Functional analysis showed that “Carbohydrate metabolism” was the most abundant metabolic category. The feature of carbohydrate-active enzymes (CZs) was analyzed using the Carbohydrate-Active EnZymes Database. The significant differences of CZs between mangrove and non-mangrove sediments, were attributed to the amounts of polyphenol oxidase (EC 1.10.3.-), hexosyltransferase (EC 2.4.1.-), and β-N-acetylhexosaminidase (EC 3.2.1.52), which were higher in the mangrove sediment samples. Principal component analysis indicated that the microbial community and gene profile between mangrove and non-mangrove sediments were distinct. Redundancy analysis showed that total organic carbon is a significant factor that affects the microbial community and gene distribution. The results indicated that the mangrove ecosystem with massive amounts of organic carbon may promote the richness of carbohydrate metabolism genes and enhance the degradation and utilization of carbohydrates in the mangrove sediments.

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References

  • Alias, S.A., Kuthubutheen, A.J., and Jones, E.B.G. 1995. Frequency of occurrence of fungi on wood in Malaysian mangroves. Hydrobiologia 295, 97–106.

    Article  Google Scholar 

  • Alongj, D.M., Boto, K.G., and Tirendi, F. 1989. Effect of exported mangrove litter on bacterial productivity and dissolved organic carbon fluxes in adjacent tropical nearshore sediments. Mar. Ecol. Prog. Ser. 56, 133–144.

    Article  Google Scholar 

  • Alongj, D.M., Christoffersen, P., and Tirendi, F. 1993. The influence of forest type on microbial-nutrient relationships in tropical mangrove sediments. J. Exp. Mar. Biol. Ecol. 171, 201–223.

    Article  Google Scholar 

  • Alzubaidy, H., Essack, M., Malas, T.B., Bokhari, A., Motwalli, O., Kamanu, F.K., Jamhor, S.A., Mokhtar, N.A., Antunes, A., Simoes, M.F., et al. 2016. Rhizosphere microbiome metagenomics of gray mangroves (Avicennia marina) in the Red Sea. Gene 576, 626–636.

    Article  CAS  PubMed  Google Scholar 

  • Andreote, F.D., Jimenez, D.J., Chaves, D., Dias, A.C.F., Luvizotto, D.M., Dini-Andreote, F., Fasanella, C.C., Lopez, M.V., Baena, S., Taketani, R.G., et al. 2012. The microbiome of Brazilian mangrove sediments as revealed by metagenomics. PLoS One 7, e38600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arfi, Y., Chevret, D., Henrissat, B., Berrin, J.G., Levasseur, A., and Record, E. 2013. Characterization of salt-adapted secreted lignocellulolytic enzymes from the mangrove fungus Pestalotiopsis sp. Nat. Commun. 4, 1810.

    Article  CAS  PubMed  Google Scholar 

  • Artimo, P., Jonnalagedda, M., Arnold, K., Baratin, D., Csardi, G., de Castro, E., Duvaud, S., Flegel, V., Fortier, A., Gasteiger, E., et al. 2012. ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res. 40, W597–W603.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badhai, J., Ghosh, T.S., and Das, S.K. 2016. Composition and functional characterization of microbiome associated with mucus of the coral Fungia echinata collected from Andaman Sea. Front. Microbiol. 7, 936.

    PubMed  PubMed Central  Google Scholar 

  • Badur, A.H., Jagtap, S.S., Yalamanchili, G., Lee, J.K., Zhao, H., and Rao, C.V. 2015. Alginate lyases from alginate-degrading Vibrio splendidus 12B01 are endolytic. Appl. Environ. Microbiol. 81, 1865–1873.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bano, N., Nisa, M., Khan, N., Saleem, M., Harrison, P., Ahmed, S., and Azam, F. 1997. Significance of bacteria in the flux of organic matter in the tidal creeks of the mangrove ecosystem of the Indus River delta, Pakistan. Mar. Ecol. Prog. Ser. 157, 1–12.

    Article  CAS  Google Scholar 

  • Barbier, E.B., Hacker, S.D., Kennedy, C., Koch, E.W., Stier, A.C., and Silliman, B.R. 2011. The value of estuarine and coastal ecosystem services. Ecol. Monogr. 81, 169–193.

    Article  Google Scholar 

  • Bashan, Y. and Holguin, G. 2002. Plant growth-promoting bacteria: a potential tool for arid mangrove reforestation. Trees 16, 159–166.

    Article  CAS  Google Scholar 

  • Beloqui, A., Pita, M., Polaina, J., Martinez-Arias, A., Golyshina, O.V., Zumarraga, M., Yakimov, M.M., Garcia-Arellano, H., Alcalde, M., Fernandez, V.M., et al. 2006. Novel polyphenol oxidase mined from a metagenome expression library of bovine rumen. J. Biol. Chem. 281, 22933–22942.

    Article  CAS  PubMed  Google Scholar 

  • Bouillon, S., Koedam, N., Raman, A., and Dehairs, F. 2002. Primary producers sustaining macro-invertebrate communities in inter-tidal mangrove forests. Oecologia 130, 441–448.

    Article  CAS  PubMed  Google Scholar 

  • Bouma, T.J., van Belzen, J., Balke, T., Zhu, Z., Airoldi, L, Blight, A.J., Davies, A.J., Galvan, C., Hawkins, S.J., Hoggart, S.P.G., et al. 2014 Identifying knowledge gaps hampering application of intertidal habitats in coastal protection: Opportunities & steps to take. Coast. Eng 87, 147–157.

    Article  Google Scholar 

  • Brune, A. 2018. Elusimicrobia, pp. 1–3. In Whitman, W.B., Rainey, E., Kampfer, P., Trujillo, M., Chun, J., DeVos, P., Hedlund, B., and Dedysh, S. (eds.), Bergey’s manual of systematics of archaea and bacteria-2015. John Wiley & Sons Ltd., Chichester, UK.

    Google Scholar 

  • Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K, and Madden, T.L. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10, 421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cantarel, B.L., Coutinho, P.M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. 2009. The carbohydrate-active enzymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 37, D233–D238.

    Article  CAS  PubMed  Google Scholar 

  • Costa, P.S., Reis, M.P., Avila, M.P., Leite, L.R., de Araujo, F.M.G., Salim, A.C.M., Oliveira, G., Barbosa, F., Chartone-Souza, E., and Nascimento, A.M.A. 2015. Metagenome of a microbial community inhabiting a metal-rich tropical stream sediment. PLoS One 10, e0119465.

  • Dias, A.C.F., Andreote, F.D., Dini-Andreote, F., Lacava, P.T., Sa, A.LB., Melo, I.S., Azevedo, J.L., and Araujo, W.L. 2009. Diversity and biotechnological potential of culturable bacteria from Brazilian mangrove sediment. World J. Microbiol. Biotechnol. 25, 1305–1311.

    Article  CAS  Google Scholar 

  • Dixon, P. 2003. VEGAN, a package of R functions for community ecology. J. Veg Sci. 14, 927–930.

    Article  Google Scholar 

  • Fang, H., Cai, L., Yang, Y., Ju, F., Li, X., Yu, Y., and Zhang, T. 2014. Metagenomic analysis reveals potential biodegradation pathways of persistent pesticides in freshwater and marine sediments. Sci. Total Environ. 470–471, 983–992.

    Google Scholar 

  • Fernandez, N.F., Gundersen, G.W., Rahman, A., Grimes, MX., Ri-kova, K., Hornbeck, P., and Ma’ayan, A. 2017. Clustergrammer, a web-based heatmap visualization and analysis tool for high-dimensional biological data. Sci. Data 4, 170151.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fu, L., Niu, B., Zhu, Z, Wu, S., and Li, W. 2012. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ganesh, S., Parris, D.J., DeLong, E.F., and Stewart, F.J. 2014. Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone. ISME J. 8, 187–211.

    Article  CAS  PubMed  Google Scholar 

  • Giri, C., Ochieng, E., Tieszen, L.L., Zhu, Z., Singh, A., Loveland, T., Masek, J., and Duke, N. 2011. Status and distribution of mangrove forests of the world using earth observation satellite data. Glob. Ecol. Biogeogr. 20, 154–159.

    Article  Google Scholar 

  • Hamady, M., Lozupone, C. and Knight, R. 2010. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and Phylo-Chip data. ISME J. 4, 17–27.

    Article  CAS  PubMed  Google Scholar 

  • Hattenschwiler, S. and Vitousek, P.M. 2000. The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol. Evol. 15, 238–243.

    Article  CAS  PubMed  Google Scholar 

  • Hedderich, R. and Whitman, W.B. 2013. Physiology and biochemistry of the methane-producing archaea, pp. 635–662. In Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F. (eds.), The prokaryotes-2013. Springer Berlin Heidelberg, Berlin, Heidelberg, Germany.

    Chapter  Google Scholar 

  • Holguin, G., Vazquez, P., and Bashan, Y. 2001. The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol. Fertil. Soils 33, 265–278.

    Article  CAS  Google Scholar 

  • Hong, K., Gao, A.H., **e, Q.Y., Gao, H.G., Zhuang, L., Lin, H.P., Yu, H.P., Li, J., Yao, X.S., Goodfellow, M., et al. 2009. Actinomycetes for marine drug discovery isolated from mangrove soils and plants in China. Mar. Drugs 7, 24–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, X.F., Bakker, M.G., Judd, T.M., Reardon, K.F., and Vivanco, J.M. 2013. Variations in diversity and richness of gut bacterial communities of termites (Reticulitermes flavipes) fed with grassy and woody plant substrates. Microb. Ecol. 65, 531–536.

    Article  PubMed  Google Scholar 

  • Huang, H., Lv, J., Hu, Y, Fang, Z., Zhang, K., and Bao, S. 2008. Micromonospora rifamycinica sp. nov., a novel actinomycete from mangrove sediment. Int. J. Syst. Evol. Microbiol. 58, 17–20.

    Article  CAS  PubMed  Google Scholar 

  • Huson, D.H., Beier, S., Flade, I., Gorska, A., El-Hadidi, M., Mitra, S., Ruscheweyh, H.J., and Tappu, R. 2016. MEGAN community edition — Interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Comput. Biol. 12, e1004957.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imchen, M., Kumavath, R., Barh, D., Vaz, A., Goes-Neto, A., Tiwari, S., Ghosh, P., Wattani, A.R., and Azevedo, V. 2018. Comparative mangrove metagenome reveals global prevalence of heavy metals and antibiotic resistome across different ecosystems. Sci. Rep. 8, 11187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang, X.T., Peng, X., Deng, G.H., Sheng, H.F., Wang, Y., Zhou, H.W., and Tarn, N.F.Y. 2013. Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland. Microb. Ecol. 66, 96–104.

    Article  PubMed  Google Scholar 

  • Kanehisa, M., Goto, S., Sato, Y., Kawashima, M., Furumichi, M., and Tanabe, M. 2014. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 42, D199–D205.

    Article  CAS  PubMed  Google Scholar 

  • Kanokratana, P., Uengwetwanit, T., Rattanachomsri, U., Bunterngsook, B., Nimchua, T., Tangphatsornruang, S., Plengvidhya, V., Champreda, V., and Eurwilaichitr, L. 2011. Insights into the phy-logeny and metabolic potential of a primary tropical peat swamp forest microbial community by metagenomic analysis. Microb. Ecol. 61, 518–528.

    Article  PubMed  Google Scholar 

  • Karlsson, F.H., Fak, F., Nookaew, I., Tremaroli, V., Fagerberg, B., Petranovic, D., Backhed, F., and Nielsen, J. 2012. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat. Commun. 3, 1245.

    Article  CAS  PubMed  Google Scholar 

  • Karlsson, F.H., Tremaroli, V., Nookaew, I., Bergstrom, G., Behre, C.J., Fagerberg, B., Nielsen, J., and Backhed, F. 2013. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498, 99–103.

    Article  CAS  PubMed  Google Scholar 

  • Kersters, K., De Vos, P., Gillis, M., Swings, J., Vandamme, P., and Stackebrandt, E. 2006. Introduction to the Proteobacteria, pp. 3–37. In Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H., and Stackebrandt, E. (eds.), The Prokaryotes-2006. Springer New York, New York, USA.

    Chapter  Google Scholar 

  • Kristensen, E., Bouillon, S., Dittmar, T., and Marchand, C. 2008. Organic carbon dynamics in mangrove ecosystems: A review. Aquat. Bot. 89, 201–219.

    Article  CAS  Google Scholar 

  • Lee, S., Cantarel, B., Henrissat, B., Gevers, D., Birren, B.W., Huttenhower, C., and Ko, G. 2014. Gene-targeted metagenomic analysis of glucan-branching enzyme gene profiles among human and animal fecal microbiota. ISME J. 8, 493–503.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Jia, H., Cai, X., Zhong, H., Feng, Q., Sunagawa, S., Arumugam, M., Kultima, J.R., Prifti, E., Nielsen, T., etal. 2014. An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 32, 834–841.

    Article  CAS  PubMed  Google Scholar 

  • Mangrola, A.V., Dudhagara, P., Koringa, P., Joshi, C.G., and Patel, R.K. 2015. Shotgun metagenomic sequencing based microbial diversity assessment of Lasundra hot spring, India. Genomics Data 4, 73–75.

    Article  PubMed  PubMed Central  Google Scholar 

  • Marcial Gomes, N.C., Borges, L.R., Paranhos, R., Pinto, F.N., Mendonca-Hagler, L.C.S., and Smalla, K. 2008. Exploring the diversity of bacterial communities in sediments of urban mangrove forests. FEMS Microbiol. Ecol. 66, 96–109.

    Article  CAS  PubMed  Google Scholar 

  • Mende, D.R., Waller, A.S., Sunagawa, S., Jarvelin, A.I., Chan, M.M., Arumugam, M., Raes, J., and Bork, P. 2012. Assessment of metagenomic assembly using simulated next generation sequencing data. PLoS One 7, e31386.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meneghine, A.K., Nielsen, S., Varani, A.M., Thomas, T., and Cara-reto Alves, L.M. 2017. Metagenomic analysis of soil and freshwater from zoo agricultural area with organic fertilization. PLoS One 12, e0190178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ministry of Agriculture of the People’s Republic of China. 2006. Method for determination of soil organic matter. NY/T 1121.6-2006. (in Chinese).

    Google Scholar 

  • Ministry of Agriculture of the People’s Republic of China. 2007. Determination of pH in soil. NY/T 1377-2007. (in Chinese).

    Google Scholar 

  • Ministry of Ecology and Environment of the People’s Republic of China. 1997. Soil quality-determination of copper, zinc-flame atomic absorption spectrophotometry. GBT 17138–1997. (in Chinese).

    Google Scholar 

  • Ministry of Ecology and Environment of the People’s Republic of China. 2016. Soil and sediment-determination of aqua regia extracts of 12 metal elements-inductively coupled plasma mass spectrometry. HJ 803-2016. (in Chinese).

    Google Scholar 

  • Nagelkerken, I., Blaber, S.J.M., Bouillon, S., Green, P., Haywood, M., Kirton, LG., Meynecke, J.O., Pawlik, J., Penrose, H.M., Sasekumar, A., et al. 2008. The habitat function of mangroves for terrestrial and marine fauna: A review. Aquat. Bot. 89, 155–185.

    Article  Google Scholar 

  • Nielsen, H.B., Almeida, M., Juncker, AS., Rasmussen, S., Li, J., Sunagawa, S., Plichta, D.R., Gautier, L., Pedersen, A.G., Le Chatelier, E., et al. 2014. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat. Biotechnol. 32, 822–828.

    Article  CAS  PubMed  Google Scholar 

  • Olutona, G.O., Olatunji, S.O., and Obisanya, J.F. 2016. Downstream assessment of chlorinated organic compounds in the bed-sediment of Aiba Stream, Iwo, South-Western, Nigeria. Springerplus 5, 67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Opsahl, S. and Benner, R. 1999. Characterization of carbohydrates during early diagenesis of five vascular plant tissues. Org. Geochem. 30, 83–94.

    Article  CAS  Google Scholar 

  • Oren, A. 2014. The family methanosarcinaceae, pp. 259–281. In Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F. (eds.), The prokaryotes-2014. Springer Berlin Heidelberg, Berlin, Heidelberg, Germany.

    Google Scholar 

  • Parks, D.H., Tyson, G.W., Hugenholtz, P., and Beiko, R.G. 2014. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30, 3123–3124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul, R.S., Ghormade, V., and Deshpande, M.V. 2000. Chitinolytic enzymes: an exploration. Enzyme Microb. Technol. 26, 473–483.

    Article  Google Scholar 

  • Powell, S., Forslund, K., Szklarczyk, D., Trachana, K., Roth, A, Huerta-Cepas, J., Gabaldon, T., Rattei, T., Creevey, C., Kuhn, M., et al. 2014. eggNOG v4.0: nested orthology inference across 3686 organisms. Nucleic Acids Res. 42, D231–D239.

    Article  CAS  PubMed  Google Scholar 

  • Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K.S., Manichanh, C. Nielsen, T., Pons, N., Levenez, F., Yamada, T., et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glockner, F.O. 2012. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rajendran, N., Saravanakumar, K., and Kathiresan, K. 2016. Mangroves: A potent source of polysaccharides, pp. 393–399. In Kim, S.K. (ed.), Marine glycobiology: principles and applications. CRC Press, Taylor & Francis Group, Boca Raton, USA.

    Chapter  Google Scholar 

  • Ray, R., Majumder, N., Das, S., Chowdhury, C., and Jana, T.K. 2014. Biogeochemical cycle of nitrogen in a tropical mangrove ecosystem, east coast of India. Mar. Chem. 167, 33–43.

    Article  CAS  Google Scholar 

  • Ronnback, P. 1999. The ecological basis for economic value of seafood production supported by mangrove ecosystems. Ecol. Econ. 29, 235–252.

    Article  Google Scholar 

  • Sahoo, K. and Dhal, N.K. 2009. Potential microbial diversity in mangrove ecosystems:A review. Indian J. Mar. Sci. 38, 249–256.

    CAS  Google Scholar 

  • Simoes, M.F., Antunes, A., Ottoni, C.A., Amini, M.S., Alam, I., Alzu-baidy, H., Mokhtar, N.A., Archer, J.A.C., and Bajic, V.B. 2015. Soil and rhizosphere associated fungi in gray mangroves (Avicennia marina) from the Red Sea — A metagenomic approach. Genomics Proteomics Bioinformatics 13, 310–320.

    Article  PubMed  PubMed Central  Google Scholar 

  • Soares, F., Marcon, J., Pereira e Silva, M., Khakhum, N., Cerdeira, L, Ottoni, J., Domingos, D., Taketani, R., de Oliveira, V.M., Lima, A.O.S., et al. 2017. A novel multifunctional β-N-acetylhexosa-minidase revealed through metagenomics of an oil-spilled mangrove. Bio engineering 4, 62.

    Google Scholar 

  • Standardization Administration of the People’s Republic of China. 2008. Soil quality — Analysis of total mercury, arsenic and lead contents in soils — Atomic fluorescence spectrometry — Part 1: analysis of total mercury contents in soils. GB/T 22105.1-2008. (in Chinese).

    Google Scholar 

  • Standardization Administration of the People’s Republic of China. 2008. Soil quality — Analysis of total mercury, arsenic and lead contents in soils — Atomic fluorescence spectrometry — Part 2: Analysis of total arsenic contents in soils. GB/T 22105.2-2008. (in Chinese).

    Google Scholar 

  • Thatoi, H., Behera, B.C., Mishra, R.R., and Dutta, S.K. 2013. Biodiversity and biotechnological potential of microorganisms from mangrove ecosystems: a review. Ann. Microbiol. 63, 1–19.

    Article  CAS  Google Scholar 

  • Thompson, C., Beys-da-Silva, W., Santi, L., Berger, M., Vainstein, M., Guima raes, J., and Vasconcelos, A.T. 2013. A potential source for cellulolytic enzyme discovery and environmental aspects revealed through metagenomics of Brazilian mangroves. AMB Express 3, 65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson, F.L., Iida, T., and Swings, J. 2004. Biodiversity of vibrios. Microbiol. Mol. Biol. Rev. 68, 403–431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walters, B.B., Ronnback, P., Kovacs, J.M., Crona, B., Hussain, S.A., Badola, R., Primavera, J.H., Barbier, E., and Dahdouh-Guebas, F. 2008. Ethnobiology, socio-economics and management of mangrove forests: A review. Aquat. Bot. 89, 220–236.

    Article  Google Scholar 

  • Wong, M.T., Wang, W., Lacourt, M., Couturier, M., Edwards, E.A., and Master, E.R. 2016. Substrate-driven convergence of the microbial community in lignocellulose-amended enrichments of gut microflora from the Canadian beaver (Castor canadensis) and north American moose (Alces americanus). Front. Microbiol. 7, 961.

    PubMed  PubMed Central  Google Scholar 

  • Yang, Q., Sun, F., Yang, Z., and Li, H. 2014. Comprehensive transcriptome study to develop molecular resources of the copepod Calanus sinicus for their potential ecological applications. Biomed Res. Int. 2014, 1–12.

    Google Scholar 

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Acknowledgements

This research was supported by the National Natural Science Foundation of China (Grant no. 31760437), the Science and Technology Basic Resources Investigation Program of China (Grant no. 2017FY100704), the Open Research Fund Program of Guangxi Key Lab of Mangrove Conservation and Utilization (Grant no. GKLMC-201702), the Distinguished Employment Offered Unit of Guangxi for Conservation and Ecological Monitoring of Mangroves and Seagrasses, the Natural Science Foundation of Guangxi Zhuang Autonomous Region of China (Grant no. 2017GXNSFAA198081, 2017-JJB130020).

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  1. State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, College of Life Science and Technology, Guangxi University, Guangxi, 530004, P. R. China

    Huaxian Zhao, Shuming Mo, Shiqing Nie, Quanwen Li, Qian Ou, Bo Wu & Chengjian Jiang

  2. Guangxi Key Laboratory of Mangrove Conservation and Utilization, Guangxi Mangrove Research Center, Guangxi Academy of Sciences, Guangxi, 536000, P. R. China

    Bing Yan & Chengjian Jiang

  3. Key Laboratory of Environment Change and Resources Use in Beibu Gulf (Guangxi Teachers Education University), Ministry of Education, Guangxi, 530001, P. R. China

    Gonglingxia Jiang, **li Tang & Nan Li

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  1. Huaxian Zhao
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Correspondence to Nan Li or Chengjian Jiang.

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Zhao, H., Yan, B., Mo, S. et al. Carbohydrate metabolism genes dominant in a subtropical marine mangrove ecosystem revealed by metagenomics analysis. J Microbiol. 57, 575–586 (2019). https://doi.org/10.1007/s12275-019-8679-5

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