[en] Bacteria degrading algal polysaccharides are key players in the global carbon cycle and in algal biomass recycling. Yet the water column, which has been studied largely by metagenomic approaches, is poor in such bacteria and their algal-polysaccharide-degrading enzymes. Even more surprisingly, the few published studies on seaweed-associated microbiomes have revealed low abundances of such bacteria and their specific enzymes. However, as macroalgal cell-wall polysaccharides do not accumulate in nature, these bacteria and their unique polysaccharidases must not be that uncommon. We, therefore, looked at the polysaccharide-degrading activity of the cultivable bacterial subpopulation associated with Ascophyllum nodosum. From A. nodosum triplicates, 324 bacteria were isolated and taxonomically identified. Out of these isolates, 78 (∼25%) were found to act on at least one tested algal polysaccharide (agar, ι- or κ-carrageenan, or alginate). The isolates “active” on algal-polysaccharides belong to 11 genera: Cellulophaga, Maribacter, Algibacter, and Zobellia in the class Flavobacteriia (41) and Pseudoalteromonas, Vibrio, Cobetia, Shewanella, Colwellia, Marinomonas, and Paraglaceciola in the class Gammaproteobacteria (37). A major part represents likely novel species. Different proportions of bacterial phyla and classes were observed between the isolated cultivable subpopulation and the total microbial community previously identified on other brown algae. Here, Bacteroidetes and Gammaproteobacteria were found to be the most abundant and some phyla (as Planctomycetes and Cyanobacteria) frequently encountered on brown algae weren’t identified. At a lower taxonomic level, twelve genera, well-known to be associated with algae (with the exception for Colwellia), were consistently found on all three A. nosodum samples. Even more interesting, 9 of the 11 above mentioned genera containing polysaccharolytic isolates were predominant in this common core. The cultivable fraction of the bacterial community associated with A. nodosum is, thus, significantly enriched in macroalgal-polysaccharide-degrading bacteria and these bacteria seem important for the seaweed holobiont even though they are under-represented in alga-associated microbiome studies.
Disciplines :
Microbiology
Author, co-author :
Martin, Marjolaine ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbiologie et génomique
Barbeyron, Tristan
Martin, Renée ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbiologie et génomique
Portetelle, Daniel ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbiologie et génomique
Michel, Gurvan
Vandenbol, Micheline ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbiologie et génomique
Language :
English
Title :
The cultivable surface microbiota of the brown alga Ascophyllum nodosum is enriched in macroalgal-polysaccharide-degrading bacteria
Publication date :
December 2015
Journal title :
Frontiers in Microbiology
eISSN :
1664-302X
Publisher :
Frontiers Research Foundation, Lausanne, Switzerland
Akagawa-Matsushita, M., Matsuo, M., Koga, Y., and Yamasato, K. (1992). Alteromonas atlantica sp. nov. and Alteromonas carrageenovora sp. nov., bacteria that decompose algal polysaccharides. Int. J. Syst. Bacteriol. 42, 621-627. doi: 10.1099/00207713-42-4-621
Barbeyron, T., Carpentier, F., L'Haridon, S., Schüler, M., Michel, G., and Amann, R. (2008). Description of maribacter forsetii sp. nov., a marine Flavobacteriaceae isolated from North Sea water, and emended description of the genus Maribacter. Int. J. Syst. Evol. Microbiol. 58, 790-797. doi: 10.1099/ijs.0.65469-0
Barbeyron, T., L'Haridon, S., Corre, E., Kloareg, B., and Potin, P. (2001). Zobellia galactanovorans gen. nov., sp. nov., a marine species of Flavobacteriaceae isolated from a red alga, and classification of [Cytophaga] uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Zobellia uliginosa gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 51, 985-997. doi: 10.1099/00207713-51-3-985
Barbeyron, T., Michel, G., Potin, P., Henrissat, B., and Kloareg, B. (2000). Iota-Carrageenases constitute a novel family of glycoside hydrolases, unrelated to that of kappa-carrageenases. J. Biol. Chem. 275, 35499-35505. doi: 10.1074/jbc.M003404200
Bengtsson, M. M., and Øvreås, L. (2010). Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol. 10:261. doi: 10.1186/1471-2180-10-261
Bengtsson, M. M., Sjøtun, K., Lanzén, A., and Øvreås, L. (2012). Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea. ISME J. 6, 2188-2198. doi: 10.1038/ismej.2012.67
Browman, J. P. (2013). "The family colwelliaceae, " in The Prokaryotes: Gammaproteobacteria, eds E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt, and F. Thompson (Berlin; Heidelberg: Springer), 179-195.
Bulgarelli, D., Schlaeppi, K., Spaepen, S., Ver Loren van Themaat, E., and Schulze-Lefert, P. (2013). Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64, 807-838. doi: 10.1146/annurev-arplant-050312-120106
Burke, C., Thomas, T., Lewis, M., Steinberg, P., and Kjelleberg, S. (2011). Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J. 5, 590-600. doi: 10.1038/ismej.2010.164
Chan, E. C., and McManus, E. A. (1969). Distribution, characterization, and nutrition of marine microorganisms from the algae Polysiphonia lanosa and Ascophyllum nodosum. Can. J. Microbiol. 15, 409-420. doi: 10.1139/m69-073
Chi, W. J., Park, J. S., Kang, D. K., and Hong, S. K. (2014). Production and characterization of a novel thermostable extracellular agarase from Pseudoalteromonas hodoensis newly isolated from the west sea of South Korea. Appl. Biochem. Biotechnol. 173, 1703-1716. doi: 10.1007/s12010-014-0958-3
Colin, S., Deniaud, E., Jam, M., Descamps, V., Chevolot, Y., Kervarec, N., et al. (2006). Cloning and biochemical characterization of the fucanase FcnA: definition of a novel glycoside hydrolase family specific for sulfated fucans. Glycobiology 16, 1021-1032. doi: 10.1093/glycob/cwl029
Cundell, A. M., Sleeter, T. D., and Mitchell, R. (1977). Microbial populations associated with the surface of the brown alga ascophyllum nodosum. Microb. Ecol. 4, 81-91. doi: 10.1007/BF02010431
DeAngelis, K. M., Gladden, J. M., Allgaier, M., D'haeseleer, P., Fortney, J. L., Reddy, A., et al. (2010). Strategies for enhancing the effectiveness of metagenomic-based enzyme discovery in lignocellulolytic microbial communities. Bioenerg. Res. 3, 146-158. doi: 10.1007/s12155-010-9089-z
de Oliveira, L., Gregoracci, G., Silva, G. G., Salgado, L., Filho, G., Alves-Ferreira, M., et al. (2012). Transcriptomic analysis of the red seaweed Laurencia dendroidea (Florideophyceae, Rhodophyta) and its microbiome. BMC Genomics 13:487. doi: 10.1186/1471-2164-13-487
Dixon, P. (2003). VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927-930. doi: 10.1111/j.1654-1103.2003.tb02228.x
Dong, S., Yang, J., Zhang, X. Y., Shi, M., Song, X. Y., Chen, X. L., et al. (2012). Cultivable alginate lyase-excreting bacteria associated with the arctic brown alga Laminaria. Mar. Drugs 10, 2481-2491. doi: 10.3390/md10112481
Egan, S., Fernandes, N. D., Kumar, V., Gardiner, M., and Thomas, T. (2014). Bacterial pathogens, virulence mechanism and host defence in marine macroalgae. Environ. Microbiol. 16, 925-938. doi: 10.1111/1462-2920.12288
Egan, S., Harder, T., Burke, C., Steinberg, P., Kjelleberg, S., and Thomas, T. (2013). The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol. Rev. 37, 462-476. doi: 10.1111/1574-6976.12011
Fernandes, N., Steinberg, P., Rusch, D., Kjelleberg, S., and Thomas, T. (2012). Community structure and functional gene profile of bacteria on healthy and diseased thalli of the red seaweed Delisea pulchra. PLoS ONE 7:e50854. doi: 10.1371/journal.pone.0050854
Ferrer, M., Martínez-Martínez, M., Bargiela, R., Streit, W. R., Golyshina, O. V., and Golyshin, P. N. (2015). Estimating the success of enzyme bioprospecting through metagenomics: current status and future trends. Microb. Biotechnol. doi: 10.1111/1751-7915.12309. [Epub ahead of print]. Available online at: http://onlinelibrary.wiley.com/doi/10.1111/1751-7915.12309/abstract
Flament, D., Barbeyron, T., Jam, M., Potin, P., Czjzek, M., Kloareg, B., et al. (2007). Alpha-agarases define a new family of glycoside hydrolases, distinct from beta-agarase families. Appl. Environ. Microbiol. 73, 4691-4694. doi: 10.1128/AEM.00496-07
Gibson, D. M., King, B. C., Hayes, M. L., and Bergstrom, G. C. (2011). Plant pathogens as a source of diverse enzymes for lignocellulose digestion. Curr. Opin. Microbiol. 14, 264-270. doi: 10.1016/j.mib.2011.04.002
Goecke, F., Labes, A., Wiese, J., and Imhoff, J. F. (2013). Phylogenetic analysis and antibiotic activity of bacteria isolated from the surface of two co-occurring macroalgae from the Baltic Sea. Eur. J. Phycol. 48, 47-60. doi: 10.1080/09670262.2013.767944
Goecke, F., Labes, A., Wiese, J., and Imhoff, J. (2010). Chemical interactions between marine macroalgae and bacteria. Mar. Ecol. Prog. Ser. 409, 267-299. doi: 10.3354/meps08607
Gómez-Pereira, P. R., Schüler, M., Fuchs, B. M., Bennke, C., Teeling, H., Waldmann, J., et al. (2012). Genomic content of uncultured Bacteroidetes from contrasting oceanic provinces in the North Atlantic Ocean. Environ. Microbiol. 14, 52-66. doi: 10.1111/j.1462-2920.2011.02555.x
Hehemann, J.-H., Correc, G., Barbeyron, T., Helbert, W., Czjzek, M., and Michel, G. (2010). Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464, 908-912. doi: 10.1038/nature08937
Hollants, J., Leliaert, F., De Clerck, O., and Willems, A. (2013). What we can learn from sushi: a review on seaweed-bacterial associations. FEMS Microbiol. Ecol. 83, 1-16. doi: 10.1111/j.1574-6941.2012.01446.x
Ivanova, E. P., Alexeeva, Y. V., Flavier, S., Wright, J. P., Zhukova, N. V., Gorshkova, N. M., et al. (2004a). Formosa algae gen. nov., sp. nov., a novel member of the family Flavobacteriaceae. Int. J. Syst. Evol. Microbiol. 54, 705-711. doi: 10.1099/ijs.0.02763-0
Ivanova, E. P., Gorshkova, N. M., Bowman, J. P., Lysenko, A. M., Zhukova, N. V., Sergeev, A. F., et al. (2004b). Shewanella pacifica sp. nov., a polyunsaturated fatty acid-producing bacterium isolated from sea water. Int. J. Syst. Evol. Microbiol. 54, 1083-1087. doi: 10.1099/ijs.0.02993-0
Ivanova, E. P., Sawabe, T., Gorshkova, N. M., Svetashev, V. I., Mikhailov, V. V., Nicolau, D. V., et al. (2001). Shewanella japonica sp. nov. Int. J. Syst. Evol. Microbiol. 51, 1027-1033. doi: 10.1099/00207713-51-3-1027
Ivanova, E. P., Sawabe, T., Hayashi, K., Gorshkova, N. M., Zhukova, N. V., Nedashkovskaya, O. I., et al. (2003). Shewanella fidelis sp. nov., isolated from sediments and sea water. Int. J. Syst. Evol. Microbiol. 53, 577-582. doi: 10.1099/ijs.0.02198-0
Johansen, J. E., Nielsen, P., and Sjraholm, C. (1999). Description of Cellulophaga baltica gen. nov., sp. nov. and Cellulophaga fucicola gen. nov., sp. nov. and reclassification of [Cytophaga] Iytica to Cellulophaga lytica gen. nov., comb. nov. Int. J. Syst. Bacteriol. 49, 1231-1240. doi: 10.1099/00207713-49-3-1231
Kim, D., Baik, K. S., Hwang, Y. S., Choi, J. S., Kwon, J., and Seong, C. N. (2013). Vibrio hemicentroti sp. nov., an alginate lyase-producing bacterium, isolated from the gut microflora of sea urchin (Hemicentrotus pulcherrimus). Int. J. Syst. Evol. Microbiol. 63, 3697-3703. doi: 10.1099/ijs.0.047951-0
Kim, M., Oh, H.-S., Park, S.-C., and Chun, J. (2014). Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int. J. Syst. Evol. Microbiol. 64, 346-351. doi: 10.1099/ijs.0.059774-0
Kim, O. S., Cho, Y. J., Lee, K., Yoon, S. H., Kim, M., Na, H., et al. (2012). Introducing EzTaxon-e: a prokaryotic 16s rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62, 716-721. doi: 10.1099/ijs.0.038075-0
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120. doi: 10.1007/BF01731581
Krieg, N. R., Staley, J. T., Brown, D. R., Hedlund, B. P., Paster, B. J., Ward, N. L., et al. (2011). Bergey's Manual® of Systematic Bacteriology: The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes, 2nd Edn., Vol.4. New York, NY; Dordrecht; Heidelberg; London: Springer.
Lachnit, T., Meske, D., Wahl, M., Harder, T., and Schmitz, R. (2011). Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ. Microbiol. 13, 655-665. doi: 10.1111/j.1462-2920.2010.02371.x
Lee, H. S., Kwon, K. K., Kang, S. G., Cha, S.-S., Kim, S.-J., and Lee, J.-H. (2010). Approaches for novel enzyme discovery from marine environments. Curr. Opin. Biotechnol. 21, 353-357. doi: 10.1016/j.copbio.2010.01.015
Leung, H. T. C., Maas, K. R., Wilhelm, R. C., and Mohn, W. W. (2015). Long-term effects of timber harvesting on hemicellulolytic microbial populations in coniferous forest soils. ISME J. doi: 10.1038/ismej.2015.118. [Epub ahead of print]. Available online at: http://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2015118a.html
Liu, Y., Liu, L.-Z., Zhong, Z.-P., Zhou, Y.-G., Liu, Y., and Liu, Z.-P. (2014). Colwellia aquaemaris sp. nov., isolated from the Cynoglossus semilaevis culture tank in a recirculating mariculture system. Int. J. Syst. Evol. Microbiol. 64, 3926-3930. doi: 10.1099/ijs.0.063305-0
Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M., and Henrissat, B. (2014). The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490-D495. doi: 10.1093/nar/gkt1178
Lucas-Elió, P., Marco-Noales, E., Espinosa, E., Ordax, M., López, M. M., Garcías-Bonet, N., et al. (2011). Marinomonas alcarazii sp. nov., M. rhizomae sp. nov., M. foliarum sp. nov., M. posidonica sp. nov. and M. aquiplantarum sp. nov., isolated from the microbiota of the seagrass Posidonia oceanica. Int. J. Syst. Evol. Microbiol. 61, 2191-2196. doi: 10.1099/ijs.0.027227-0
Macián, M. C., Arahal, D. R., Garay, E., and Pujalte, M. J. (2005). Marinomonas aquamarina sp. nov., isolated from oysters and seawater. Syst. Appl. Microbiol. 28, 145-150. doi: 10.1016/j.syapm.2004.12.003
Mann, A. J., Hahnke, R. L., Huang, S., Werner, J., Xing, P., Barbeyron, T., et al. (2013). The genome of the alga-associated marine flavobacterium Formosa agariphila KMM 3901T reveals a broad potential for degradation of algal polysaccharides. Appl. Environ. Microbiol. 79, 6813-6822. doi: 10.1128/AEM.01937-13
Martin, M., Biver, S., Steels, S., Barbeyron, T., Jam, M., Portetelle, D., et al. (2014a). Identification and characterization of a halotolerant, cold-active marine endo-beta-1, 4-glucanase by using functional metagenomics of seaweed-associated microbiota. Appl. Environ. Microbiol. 80, 4958-4967. doi: 10.1128/AEM.01194-14
Martin, M., Portetelle, D., Michel, G., and Vandenbol, M. (2014b). Microorganisms living on macroalgae: diversity, interactions, and biotechnological applications. Appl. Microbiol. Biotechnol. 98, 2917-2935. doi: 10.1007/s00253-014-5557-2
Marzinelli, E. M., Campbell, A. H., Zozaya Valdes, E., Vergés, A., Nielsen, S., Wernberg, T., et al. (2015). Continental-scale variation in seaweed host-associated bacterial communities is a function of host condition, not geography. Environ. Microbiol. 17, 4078-4088. doi: 10.1111/1462-2920.12972
Matsuo, Y., Suzuki, M., Kasai, H., Shizuri, Y., and Harayama, S. (2003). Isolation and phylogenetic characterization of bacteria capable of inducing differentiation in the green alga Monostroma oxyspermum. Environ. Microbiol. 5, 25-35. doi: 10.1046/j.1462-2920.2003.00382.x
Michel, G., Chantalat, L., Duee, E., Barbeyron, T., Henrissat, B., Kloareg, B., et al. (2001). The kappa-carrageenase of P. carrageenovora features a tunnel-shaped active site: a novel insight in the evolution of Clan-B glycoside hydrolases. Structure 9, 513-525. doi: 10.1016/S0969-2126(01)00612-8
Michel, G., and Czjzek, M. (2013). "Polysaccharide-degrading enzymes from marine bacteria, " in Marine Enzymes for Biocatalysis:Sources, Biocatalytic Characteristic and Bioprocesses of Marine Enzymes, ed A. Trincone (Cambridge: Woodhead Publishing Limited), 429-464.
Nadkarni, M., A., Martin, F. E., Jacques, N., A., and Hunter, N. (2002). Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148, 257-266. doi: 10.1099/00221287-148-1-257
Nedashkovskaya, O. I. (2006). Formosa agariphila sp. nov., a budding bacterium of the family Flavobacteriaceae isolated from marine environments, and emended description of the genus Formosa. Int. J. Syst. Evol. Microbiol. 56, 161-167. doi: 10.1099/ijs.0.63875-0
Nedashkovskaya, O. I., Suzuki, M., Vancanneyt, M., Cleenwerck, I., Lysenko, A. M., Mikhailov, V. V., et al. (2004). Zobellia amurskyensis sp. nov., Zobellia laminariae sp. nov. and Zobellia russellii sp. nov., novel marine bacteria of the family Flavobacteriaceae. Int. J. Syst. Evol. Microbiol. 54, 1643-1648. doi: 10.1099/ijs.0.63091-0
Neumann, A. M., Balmonte, J. P., Berger, M., Giebel, H.-A., Arnosti, C., Voget, S., et al. (2015). Different utilization of alginate and other algal polysaccharides by marine Alteromonas macleodii ecotypes. Environ. Microbiol. 17, 3857-3868. doi: 10.1111/1462-2920.12862
Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Simpson, G. L., Solymos, P., et al. (2008). The Vegan Package. Community Ecology package. 1-174. Available online at: http://vegan.r-forge.r-project.org/
Olsen, J. L., Zechman, F. W., Hoarau, G., Coyer, J. A., Stam, W. T., Valero, M., et al. (2010). The phylogeographic architecture of the fucoid seaweed Ascophyllum nodosum: an intertidal "marine tree" and survivor of more than one glacial-interglacial cycle. J. Biogeogr. 37, 842-856. doi: 10.1111/j.1365-2699.2009.02262.x
Park, S. C., Hwang, Y. M., Lee, J. H., Baik, K. S., and Seong, C. N. (2013). Algibacter agarivorans sp. nov. and Algibacter agarilyticus sp. nov., isolated from seawater, reclassification of Marinivirga aestuarii as Algibacter aestuarii comb. nov. and emended description of the genus Algibacter. Int. J. Syst. Evol. Microbiol. 63, 3494-3500. doi: 10.1099/ijs.0.051300-0
Park, S., Oh, K. H., Lee, S. Y., Oh, T. K., and Yoon, J. H. (2012). Cellulophaga geojensis sp. nov., a member of the family Flavobacteriaceae isolated from marine sand. Int. J. Syst. Evol. Microbiol. 62, 1354-1358. doi: 10.1099/ijs.0.033340-0
Popper, Z. A, Michel, G., Hervé, C., Domozych, D. S., Willats, W. G. T., Tuohy, M. G., et al. (2011). Evolution and diversity of plant cell walls: from algae to flowering plants. Annu. Rev. Plant Biol. 62, 567-590. doi: 10.1146/annurev-arplant-042110-103809
Potin, P., Bouarab, K., Salaün, J.-P., Pohnert, G., and Kloareg, B. (2002). Biotic interactions of marine algae. Curr. Opin. Plant Biol. 5, 308-317. doi: 10.1016/S1369-5266(02)00273-X
Rebuffet, E., Groisillier, A., Thompson, A., Jeudy, A., Barbeyron, T., Czjzek, M., et al. (2011). Discovery and structural characterization of a novel glycosidase family of marine origin. Environ. Microbiol. 13, 1253-1270. doi: 10.1111/j.1462-2920.2011.02426.x
Romanenko, L. A., Zhukova, N. V., Rohde, M., Lysenko, A. M., Mikhailov, V. V., and Stackebrandt, E. (2003). Glaciecola mesophila sp. nov., a novel marine agar-digesting bacterium. Int. J. Syst. Evol. Microbiol. 53, 647-651. doi: 10.1099/ijs.0.02469-0
Saitou, N., and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
Stackebrandt, E. (2011). Molecular taxonomic parameters. Microbiol. Aust. 32, 59-61. Available online at: http://microbiology.publish.csiro.au/?paper=MA11059
Stratil, S. B., Neulinger, S. C., Knecht, H., Friedrichs, A. K., and Wahl, M. (2013). Temperature-driven shifts in the epibiotic bacterial community composition of the brown macroalga Fucus vesiculosus. Microbiologyopen 2, 338-349. doi: 10.1002/mbo3.79
Stratil, S. B., Neulinger, S. C., Knecht, H., Friedrichs, A. K., and Wahl, M. (2014). Salinity affects compositional traits of epibacterial communities on the brown macroalga Fucus vesiculosus. FEMS Microbiol. Ecol. 88, 272-279. doi: 10.1111/1574-6941.12292
Stroobants, A., Degrune, F., Olivier, C., Muys, C., Roisin, C., Colinet, G., et al. (2014). Diversity of bacterial communities in a profile of a winter wheat field: known and unknown members. Microb. Ecol. 68, 822-833. doi: 10.1007/s00248-014-0458-6
Sugano, Y., Matsumoto, T., Kodama, H., and Noma, M. (1993). Cloning and sequencing of agaa, a unique agarase 0107 gene from a marine bacterium, vibrio sp. strain JT0107. Appl. Environ. Microbiol. 59, 3750-3756.
Tanaka, R., Shibata, T., Miyake, H., Mori, T., Tamaru, Y., Ueda, M., et al. (2015). Temporal fluctuation in the abundance of alginate-degrading bacteria in the gut of abalone Haliotis gigantea over 1 year. Aquac. Res. doi: 10.1111/are.12740. [Epub ahead of print]. Available online at: http://onlinelibrary.wiley.com/doi/10.1111/are.12740/references
Tindall, B. J., Rosselló-Móra, R., Busse, H. J., Ludwig, W., and Kämpfer, P. (2010). Notes on the characterization of prokaryote strains for taxonomic purposes. Int. J. Syst. Evol. Microbiol. 60, 249-266. doi: 10.1099/ijs.0.016949-0
Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L., Rusch, D., Eisen, J. A., et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66-74. doi: 10.1126/science.1093857
Wang, F.-Q., Lin, X.-Z., Chen, G.-J., and Du, Z.-J. (2015). Colwellia arctica sp. nov., isolated from Arctic marine sediment. Antonie Van Leeuwenhoek 107, 723-729. doi: 10.1007/s10482-014-0366-2
Wang, L., Li, S., Yu, W., and Gong, Q. (2014). Cloning, overexpression and characterization of a new oligoalginate lyase from a marine bacterium, Shewanella sp. Biotechnol. Lett. 37, 665-671. doi: 10.1007/s10529-014-1706-z
Wiese, J., Thiel, V., Nagel, K., Staufenberger, T., and Imhoff, J. F. (2009). Diversity of antibiotic-active bacteria associated with the brown alga Laminaria saccharina from the Baltic Sea. Mar. Biotechnol. (NY). 11, 287-300. doi: 10.1007/s10126-008-9143-4
Yao, Z., Wang, F., Gao, Z., Jin, L., and Wu, H. (2013). Characterization of a κ-carrageenase from marine cellulophaga lytica strain n5-2 and analysis of its degradation products. Int. J. Mol. Sci. 14, 24592-24602. doi: 10.3390/ijms141224592
Yong, J. J., Park, S. J., Kim, H. J., and Rhee, S. K. (2007). Glaciecola agarilytica sp. nov., an agar-digesting marine bacterium from the East Sea, Korea. Int. J. Syst. Evol. Microbiol. 57, 951-953. doi: 10.1099/ijs.0.64723-0
Yooseph, S., Sutton, G., Rusch, D. B., Halpern, A. L., Williamson, S. J., Remington, K., et al. (2007). The Sorcerer II global ocean sampling expedition: expanding the universe of protein families. PLoS Biol. 5:e16. doi: 10.1371/journal.pbio.0050016
Yung, P. Y., Burke, C., Lewis, M., Kjelleberg, S., and Thomas, T. (2011). Novel antibacterial proteins from the microbial communities associated with the sponge Cymbastela concentrica and the green alga Ulva australis. Appl. Environ. Microbiol. 77, 1512-1515. doi: 10.1128/AEM.02038-10
