Microorganisms living on macroalgae: Diversity, interactions, and biotechnological applications

Applied Microbiology and Biotechnology

Volumn 98, Issue 7, 2014, Pages 2917-2935

  Martin, Marjolaine ^a   Portetelle, Daniel ^a   Michel, Gurvan ^b,c   Vandenbol, Micheline ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b SORBONNE UNIVERSITÉ   (France)

^c STATION BIOLOGIQUE DE ROSCOFF   (France)

Author keywords

Algal polysaccharidases; Algal symbiosis; Antimicrobial compounds; Glycoside hydrolases; Microbial biofilms

Indexed keywords

ALGAE; BIODIVERSITY; BIOFILMS; BIOTECHNOLOGY; ECOLOGY; GALLIUM ALLOYS; INDUSTRIAL APPLICATIONS;

ALGAL POLYSACCHARIDASES; ALGAL SYMBIOSIS; ANTIMICROBIAL COMPOUNDS; GLYCOSIDE HYDROLASES; MICROBIAL BIOFILM;

MICROORGANISMS;

AGAR; AGARASE; ALGINATE LYASE; ALGINIC ACID; ALPHA 1,3 (3,6 ANHYDRO)L GALACTOSIDASE; ANTIINFECTIVE AGENT; BIOFUEL; CARRAGEENAN; DEHALOGENASE; ENDO 1,3 BETA GLUCANASE; FUCOIDANASE; HYDROLASE; KAPPA CARRAGEENANASE; LAMINARAN; MANNITOL; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; POLYSACCHARIDASE; PORPHYRANASE; ULVAN LYASE; UNCLASSIFIED DRUG;

BIOACTIVITY; BIODIVERSITY; BIOFILM; BIOTECHNOLOGY; ENZYME ACTIVITY; INDUSTRIAL PRODUCTION; MACROALGA; MARINE ECOSYSTEM; MARINE TECHNOLOGY; METABOLITE; MICROBIAL COMMUNITY; SEAWATER; SPECIES DIVERSITY;

ACTINOBACTERIA; ALGA; ALGORIPHAGUS; ALTEROMONAS; ANTIMICROBIAL ACTIVITY; AQUAMARINA; AQUATIC ENVIRONMENT; BACILLUS; BACTERIUM; BACTEROIDETES; BIOFILM; BROWN ALGA; BRYOPSIS HYPNOIDES; CAULERPA TAXIFOLIA; CHLOROFLEXI; CRYSTAL STRUCTURE; DELESSERIA SANGUINEA; DELISEA PULCHRA; DENSITY; DICTYOTA BARTAYRESIANA; DRUG INDUSTRY; FIRMICUTES; FLAVOBACTERIACEAE; FOOD INDUSTRY; FUCUS VESICULOSUS; GLACIECOLA; GRACILERIA VERMICULOPHYLLA; GREEN ALGA; HOST PARASITE INTERACTION; JANIA RUBENS; KOPRIIMONAS; LABORATORY; LAMINARIA DIGITATA; LAMINARIA HYPERBOREA; LAMINARIA SACCHARINA; MACROALGA; MESORHIZOBIUM; METABOLITE; MICROBACTERIUM; MICROFLORA; MICROORGANISM; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT UPTAKE; PAENIBACILLUS; PAPER INDUSTRY; PARACOCCUS; PARRACOCCUS; PHAEOBACTER; PHOTOBACTERIUM; PLANCTOMYCETES; PROTEOBACTERIA; PSEUDOALTERMONAS; PSEUDOALTEROMONAS; PSEUDOMONAS; PSYCHROBACTER; RED ALGA; REVIEW; RHODOBACTERACEAE; RHODOBACTERALES; ROSEOBACTER; RUEGERI; SCHWENALLA; SEAWEED; SPECIES DIVERSITY; STREPTOMYCES; TEXTILE INDUSTRY; ULVA AUSTRALIS; ULVA INTESTINALIS; VIBRIO; ZOBELLIA;

ALGAE;

BACTERIA; BIODIVERSITY; BIOLOGICAL PRODUCTS; BIOTECHNOLOGY; SEAWEED; SYMBIOSIS;

EID: 84898888957     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5557-2     Document Type: Review

References (164)

1. Allouch J, Jam M, Helbert W, Barbeyron T, Kloareg B, Henrissat B, Czjzek M (2003) The three-dimensional structures of two beta-agarases. J Biol Chem 278:47171-47180. doi: 10.1074/jbc.M308313200
2. Allouch J, Helbert W, Henrissat B, Czjzek M (2004) Parallel substrate binding sites in a beta-agarase suggest a novel mode of action on double-helical agarose. Structure 12:623-632. doi: 10.1016/j.str.2004.02.020
3. Andrykovitch G, Marx I (1988) Isolation of a new polysaccharide-digesting bacterium from a salt marsh. Appl Environ Microbiol 54:1061-1063
4. Armstrong E, Rogerson A, Leftley JW (2000) The abundance of heterotrophic protists associated with intertidal seaweeds. Estuar Coast Shelf Sci 50:415-424. doi: 10.1006/ecss.1999.0577
5. Barbeyron T, Henrissat B, Kloareg B (1994) The gene encoding the kappa-carrageenase of Alteromonas carrageenovora is related to β-1,3-1,4-glucanases. Gene 139:105-109
6. Barbeyron T, Gerard A, Potin P, Henrissat B, Kloareg B (1998) The kappa-carrageenase of the marine bacterium Cytophaga drobachiensis. Structural and phylogenetic relationships within family-16 glycoside hydrolases. Mol Biol Evol 15:528-537
7. Barbeyron T, Michel G, Potin P, Henrissat B, 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
8. Barbeyron T, L'Haridon S, Corre E, Kloareg B, 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
9. Barbeyron T, L'Haridon S, Michel G, Czjzek M (2008) Mariniflexile fucanivorans sp. Nov., a marine member of the Flavobacteriaceae that degrades sulphated fucans from brown algae. Int J Syst Evol Microbiol 58:2107-2113. doi: 10.1099/ijs.0.65674-0
10. Barbeyron T, Lerat Y, Sassi J-F, Le Panse S, Helbert W, Collén PN (2011) Persicivirga ulvanivorans sp. Nov., a marine member of the family Flavobacteriaceae that degrades ulvan from green algae. Int J Syst Evol Microbiol 61:1899-1905. doi: 10.1099/ijs.0.024489-0
11. Barott KL, Rodriguez-Brito B, Janouškovec J, Marhaver KL, Smith JE, Keeling P, Rohwer FL (2011) Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 13:1192-1204. doi: 10.1111/j.1462-2920.2010.02419.x
12. Belas R (1989) Sequence analysis of the agrA gene encoding beta-agarase from Pseudomonas atlantica. J Bacteriol 171:602-605
13. Bengtsson MM, Øvreås L (2010) Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol 10:261. doi: 10.1186/1471-2180-10-261
14. Bengtsson M, Sjøtun K, Øvreås L (2010) Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat Microb Ecol 60:71-83. doi: 10.3354/ame01409
15. Bengtsson MM, Sjoetun K, Lanzen A, Oevreas L (2013) Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea. ISME J 6:2188-2198
16. Berteau O, Mulloy B (2003) Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology 13:29R-40R. doi: 10.1093/glycob/cwg058
17. Bhatnagar I, Kim S-K (2010) Immense essence of excellence: marine microbial bioactive compounds. Mar Drugs 8:2673-2701. doi: 10.3390/md8102673
18. Bhattacharyya S, Liu H, Zhang Z, Jam M, Dudeja PK, Michel G, Linhardt RJ, Tobacman JK (2010) Carrageenan-induced innate immune response is modified by enzymes that hydrolyze distinct galactosidic bonds. J Nutr Biochem 21:906-913. doi: 10.1016/j.jnutbio.2009.07.002
19. Bixler HJ, Porse H (2010) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321-335. doi: 10.1007/s10811-010-9529-3
20. Both H, Brown SH, Kelly RM (1993) Characterization of amylolytic enzymes, having both ox-1, 4 and ao-1, 6 hydrolytic activity, from the thermophilic archaea Pyrococcus furiosus and Thermococcus litoralis
21. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011a) Bacterial community assembly based on functional genes rather than species. PNAS 108:14288-14293. doi: 10.1073/pnas.1101591108/-/DCSupplemental.www.pnas.org/cgi/ doi/10.1073/pnas.1101591108
22. Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg S (2011b) 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
23. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233-D238. doi: 10.1093/nar/gkn663
24. Chassany O, Bonaz B, Bruley DES, Varannes S, Bueno L, Cargill G, Coffin B, Ducrotté P, Grangé V (2007) Acute exacerbation of pain in irritable bowel syndrome: efficacy of phloroglucinol/trimethylphloroglucinol. A randomized, double-blind, placebo-controlled study. Aliment Pharmacol Ther 25:1115-1123. doi: 10.1111/j.1365-2036.2007.03296.x
25. Colin S, Deniaud E, Jam M, Descamps V, Chevolot Y, Kervarec N, Yvin J-C, Barbeyron T, Michel G, Kloareg B (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
26. Corre S, Prieur D (1990) Density and morphology of epiphytic bacteria on the kelp Laminaria digitata. Bot Mar 33:515-523
27. Correc G, Hehemann J-H, Czjzek M, Helbert W (2011) Structural analysis of the degradation products of porphyran digested by Zobellia galactanivorans β-porphyranase A. Carbohydr Polym 83:277-283. doi: 10.1016/j.carbpol.2010. 07.060
28. Cosse A, Leblanc C, Potin P (2007) Dynamic defense of marine macroalgae against pathogens: from early activated to gene regulated responses. Adv Bot Res 46:221-266
29. Cristóbal HA, Schmidt A, Kothe E, Breccia J, Abate CM (2009) Characterization of inducible cold-active β-glucosidases from the psychrotolerant bacterium Shewanella sp. G5 isolated from a sub-Antarctic ecosystem. Enzym Microb Technol 45:498-506. doi: 10.1016/j.enzmictec.2009.06.010
30. Cristóbal HA, López MA, Kothe E, Abate CM (2011) Diversity of protease-producing marine bacteria from sub-antarctic environments. J Basic Microbiol 51:590-600. doi: 10.1002/jobm.201000413
31. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90-93. doi: 10.1038/nature04056
32. Croft MT, Warren MJ, Smith AG (2006) Algae need their vitamins. Eukaryot Cell 5:1175-1183. doi: 10.1128/EC.00097-06
33. Cundell AM, Sleeter TD, Mitchell R (1977) Microbial populations associated with the surface of the brown alga Ascophyllum nodosum. Microb Ecol 4:81-91
34. De Ruiter GA, Rudolph B (1997) Carrageenan biotechnology. Trends Food Sci Technol 8:389-395
35. Descamps V, Colin S, Lahaye M, Jam M, Richard C, Potin P, Barbeyron T, Yvin J-C, Kloareg B (2006) Isolation and culture of a marine bacterium degrading the sulfated fucans from marine brown algae. Mar Biotechnol (NY) 8:27-39. doi: 10.1007/s10126-005-5107-0
36. Dimitrieva GY, Crawford RL, Yuksel GU (2006) The nature of plant growth-promoting effects of a pseudoalteromonad associated with the marine algae Laminaria japonica and linked to catalase excretion. J Appl Microbiol 100:1159-1169. doi: 10.1111/j.1365-2672.2006.02831.x
37. Dobretsov S, Dahms H-U, Qian P-Y (2006) Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling 22:43-54. doi: 10.1080/08927010500504784
38. Dong J, Hashikawa S, Konishi T, Tamaru Y, Araki T (2006) Cloning of the novel gene encoding beta-agarase C from a marine bacterium, Vibrio sp. strain PO-303, and characterization of the gene product. Appl Environ Microbiol 72:6399-6401. doi: 10.1128/AEM.00935-06
39. Dong J, Hong Y, Shao Z, Liu Z (2010) Molecular cloning, purification, and characterization of a novel, acidic, pH-stable endoglucanase from Martelella mediterranea. J Microbiol 48:393-398
40. Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881-890. doi: 10.3201/eid0809.020063
41. Egan S, Thomas T, Kjelleberg S (2008) Unlocking the diversity and biotechnological potential of marine surface associated microbial communities. Curr Opin Microbiol 11:219-225. doi: 10.1016/j.mib.2008.04.001
42. Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T (2013) The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol Rev 37:462-476. doi: 10.1111/1574-6976.12011
43. Engel S, Jensen PR, Fenical W (2002) Chemical ecology of marine microbial defense. J Chem Ecol 28:1971-1985
44. Enquist-Newman M, Faust AME, Bravo DD, Santos CNS, Raisner RM, Hanel A, Sarvabhowman P, Le C, Regitsky DD, Cooper SR, Peereboom L, Clark A, Martinez Y, Goldsmith J, Cho MY, Donohoue PD, Luo L, Lamberson B, Tamrakar P, Kim EJ, Villari JL, Gill A, Tripathi SA, Karamchedu P, Paredes CJ, Rajgarhia V, Kotlar HK, Bailey RB, Miller DJ, Ohler NL, Swimmer C, Yoshikuni Y (2013) Efficient ethanol production from brown macroalgae sugars by a synthetic yeast platform. Nature. doi: 10.1038/nature12771
45. Erwin PM, Olson JB, Thacker RW (2011) Phylogenetic diversity, host-specificity and community profiling of sponge-associated bacteria in the northern Gulf of Mexico. PLoS One 6:1-16. doi: 10.1371/journal.pone.0026806
46. Fang Z-M, Li T-L, Chang F, Zhou P, Fang W, Hong Y-Z, Zhang X-C, Peng H, Xiao Y-Z (2012) A new marine bacterial laccase with chloride-enhancing, alkaline-dependent activity and dye decolorization ability. Bioresour Technol 111:36-41. doi: 10.1016/j.biortech.2012.01.172
47. Fernandes N, Steinberg P, Rusch D, Kjelleberg S, 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
48. Flament D, Barbeyron T, Jam M, Potin P, Czjzek M, Kloareg B, Michel G (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
49. Fu X, Liu P, Lin L, Hong Y, Huang X, Meng X, Liu Z (2010) A novel endoglucanase (Cel9P) from a marine bacterium Paenibacillus sp. BME-14. Appl Biochem Biotechnol 160:1627-1636
50. Gavrilescu M, Chisti Y (2005) Biotechnology - a sustainable alternative for chemical industry. Biotechnol Adv 23:471-499. doi: 10.1016/j.biotechadv. 2005.03.004
51. Ge H, Xu P, Xu Y, Fang Z, Xiao Y (2011) Purification, crystallization and preliminary crystallographic analysis of recombinant Lac15 from a marine microbial metagenome. Acta Crystallogr Sect F: Struct Biol Cryst Commun 67:956-958. doi: 10.1107/S1744309111024912
52. Genilloud O, Pelaez F, Gonzalez I, Diez MT (1994) Diversity of actinomycetes and fungi on seaweeds from the Iberian coasts. Microbiologia 10:413-422
53. Gibbs MD, Saul DJ, Lüthi E, Bergquist PL (1992) The beta-mannanase from "Caldocellum saccharolyticum" is part of a multidomain enzyme. Appl Environ Microbiol 58:3864-3867
54. Goecke F, Labes A, Wiese J, Imhoff J (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267-299. doi: 10.3354/meps08607
55. Goecke F, Labes A, Wiese J, Imhoff JF (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
56. Gontang EA, Fenical W, Jensen PR (2007) Phylogenetic diversity of gram-positive bacteria cultured from marine sediments. Appl Environ Microbiol 73:3272-3282. doi: 10.1128/AEM.02811-06
57. Gravot A, Dittami S, Rousvoal S, Lugan R, Eggert A, Collén J, Boyen C, Bouchereau A, Tonon T (2010) Diurnal oscillations of metabolite abundances and gene analysis provide new insights into central metabolic processes of the brown alga Ectocarpus siliculosus. New Phytol 188:98-110
58. Guibet M, Barbeyron T, Genicot S, Kloareg B, Michel G, Helbert W (2007) Degradation of λ-carrageenan by Pseudoalteromonas carrageenovora λ-carrageenase: a new family of glycoside hydrolases unrelated to κ- and ι-carrageenases. Biochem J 114:105-114. doi: 10.1042//BJ20061359
59. Ha SC, Lee S, Lee J, Kim HT, Ko H-J, Kim KH, Choi I-G (2011) Crystal structure of a key enzyme in the agarolytic pathway, α-neoagarobiose hydrolase from Saccharophagus degradans 2-40. Biochem Biophys Res Commun 412:238-244. doi: 10.1016/j.bbrc.2011.07.073
60. Han F, Gong Q-H, Song K, Li J-B, Yu W-G (2004) Cloning, sequence analysis and expression of gene alyVI encoding alginate lyase from marine bacterium Vibrio sp. QY101. DNA Seq 15:344-350. doi: 10.1080/10425170400019300
61. Harder T, Campbell AH, Egan S, Steinberg PD (2012) Chemical mediation of ternary interactions between marine holobionts and their environment as exemplified by the red alga Delisea pulchra. J Chem Ecol 38:442-450. doi: 10.1007/s10886-012-0119-5
62. Hatada Y, Ohta Y, Horikoshi K (2006) Hyperproduction and application of alpha-agarase to enzymatic enhancement of antioxidant activity of porphyran. J Agric Food Chem 54:9895-9900. doi: 10.1021/jf0613684
63. Hatada Y, Mizuno M, Li Z, Ohta Y (2011) Hyper-production and characterization of the ι-carrageenase useful for ι-carrageenan oligosaccharide production from a deep-sea bacterium, Microbulbifer thermotolerans JAMB-A94T, and insight into the unusual catalytic mechanism. Mar Biotechnol (NY) 13:411-422. doi: 10.1007/s10126-010-9312-0
64. Hehemann J-H, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G (2010) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464:908-912. doi: 10.1038/nature08937
65. Hehemann J-H, Correc G, Thomas F, Bernard T, Barbeyron T, Jam M, Helbert W, Michel G, Czjzek M (2012a) Biochemical and structural characterization of the complex agarolytic enzyme system from the marine bacterium Zobellia galactanivorans. J Biol Chem 287:30571-30584. doi: 10.1074/jbc.M112.377184
66. Hehemann J-H, Kelly AG, Pudlo NA, Martens EC, Boraston AB (2012b) Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc Natl Acad Sci U S A 109:19786-19791. doi: 10.1073/pnas.1211002109
67. Hehemann J-H, Smyth L, Yadav A, Vocadlo DJ, Boraston AB (2012c) Analysis of keystone enzyme in Agar hydrolysis provides insight into the degradation (of a polysaccharide from) red seaweeds. J Biol Chem 287:13985-13995. doi: 10.1074/jbc.M112.345645
68. Hollants J, Leroux O, Leliaert F, Decleyre H, De Clerck O, Willems A (2011) Who is in there? Exploration of endophytic bacteria within the siphonous green seaweed Bryopsis (Bryopsidales, Chlorophyta). PLoS One 6:e26458. doi: 10.1371/journal.pone.0026458
69. Ismail-Ben Ali A, El Bour M, Ktari L, Bolhuis H, Ahmed M, Boudabbous A, Stal LJ (2011) Jania rubens-associated bacteria: molecular identification and antimicrobial activity. J Appl Phycol 24:525-534. doi: 10.1007/s10811-011-9758-0
70. Jam M, Flament D, Allouch J, Potin P, Thion L, Kloareg B, Czjzek M, Helbert W, Michel G, Barbeyron T (2005) The endo-beta-agarases AgaA and AgaB from the marine bacterium Zobellia galactanivorans: two paralogue enzymes with different molecular organizations and catalytic behaviours. Biochem J 385:703-713. doi: 10.1042/BJ20041044
71. Jiao G, Yu G, Zhang J, Ewart HS (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9:196-223. doi: 10.3390/md9020196
72. Jiao G, Yu G, Zhao X, Zhang J, Ewart HS (2012) Natural polymers with antioxidant properties: poly-/oligosaccharides of marine origin. In: Cirilo G, Iemma F (eds) Antioxid Polym Synth Prop Appl John Wiley & Sons, Hoboken, USA, pp 179-201
73. Jung KA, Lim S-R, Kim Y, Park JM (2013) Potentials of macroalgae as feedstocks for biorefinery. Bioresour Technol 135:182-190. doi: 10.1016/j.biortech.2012.10.025
74. Kanagasabhapathy M, Sasaki H, Haldar S, Yamasaki S, Nagata S (2006) Antibacterial activities of marine epibiotic bacteria isolated from brown algae of Japan. Ann Microbiol 56:167-173. doi: 10.1007/BF03175000
75. Kanagasabhapathy M, Sasaki H, Nagata S (2008) Phylogenetic identification of epibiotic bacteria possessing antimicrobial activities isolated from red algal species of Japan. World J Microbiol Biotechnol 24:2315-2321. doi: 10.1007/s11274-008-9746-y
76. Kennedy J, O'Leary ND, Kiran GS, Morrissey JP, O'Gara F, Selvin J, Dobson ADW (2011) Functional metagenomic strategies for the discovery of novel enzymes and biosurfactants with biotechnological applications from marine ecosystems. J Appl Microbiol 111:787-799. doi: 10.1111/j.1365-2672.2011.05106.x
77. Kilian SG, Prior BA, Venter JJ, Lategan PM (1985) Production, purification, and properties of beta-glucosidase from Candida wickerhamii. Appl Microbiol Biotechnol 21:148-153
78. Kim J, Hong S-K (2012) Isolation and characterization of an agarase-producing bacterial strain, Alteromonas sp. GNUM-1, from the West Sea, Korea. J Microbiol Biotechnol 22:1621-1628. doi: 10.4014/jmb.1209.08087
79. Kim DE, Lee EY, Kim HS (2009) Cloning and characterization of alginate lyase from a marine bacterium Streptomyces sp. ALG-5. Mar Biotechnol (NY) 11:10-16
80. Kim HT, Lee S, Kim KH, Choi I-G (2012) The complete enzymatic saccharification of agarose and its application to simultaneous saccharification and fermentation of agarose for ethanol production. Bioresour Technol 107:301-306. doi: 10.1016/j.biortech.2011.11.120
81. Kobayashi T, Uchimura K, Koide O, Deguchi S, Horikoshi K (2012) Genetic and biochemical characterization of the Pseudoalteromonas tetraodonis alkaline κ-carrageenase. Biosci Biotechnol Biochem 76:506-511. doi: 10.1271/bbb.110809
82. Kubanek J, Jensen PR, Keifer PA, Sullards MC, Collins DO, Fenical W (2003) Seaweed resistance to microbial attack: a targeted chemical defense against marine fungi. Proc Natl Acad Sci U S A 100:6916-6921. doi: 10.1073/pnas.1131855100
83. Labourel A, Jam M, Jeudy A, Hehemann J-H, Czjzek M, Michel G (2014) The β-glucanase ZgLamA from Zobellia galactanivorans evolved a bent active site adapted for efficient degradation of algal laminarin. J Biol Chem 289:2027-2042. doi: 10.1074/jbc.M113.538843
84. Lachnit T, Blümel M, Imhoff J, Wahl M (2009) Specific epibacterial communities on macroalgae: phylogeny matters more than habitat. Aquat Biol 5:181-186. doi: 10.3354/ab00149
85. Lachnit T, Meske D, Wahl M, Harder T, 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
86. Lahaye M, Robic A (2007) Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765-1774. doi: 10.1021/bm061185q
87. Lahaye M, Brunel M, Bonnin E (1997) Fine chemical structure analysis of oligosaccharides produced by an ulvan-lyase degradation of the water-soluble cell-wall polysaccharides from Ulva sp, (Ulvales, Chlorophyta). Carbohydr Res 304:325-333
88. Lemoine M, Nyvall Collén P, Helbert W (2009) Physical state of kappa-carrageenan modulates the mode of action of kappa-carrageenase from Pseudoalteromonas carrageenovora. Biochem J 419:545-553. doi: 10.1042/BJ20080619
89. Lemos ML, Toranzo AE, Barja JL (1985) Antibiotic activity of epiphytic bacteria isolated from intertidal seaweeds. Microb Ecol 11:149-163. doi: 10.1007/BF02010487
90. Li B, Lu F, Wei X, Zhao R (2008) Fucoidan: structure and bioactivity. Molecules 13:1671-1695. doi: 10.3390/molecules13081671
91. Li J-W, Dong S, Song J, Li C-B, Chen X-L, Xie B-B, Zhang Y-Z (2011) Purification and characterization of a bifunctional alginate lyase from Pseudoalteromonas sp. SM0524. Mar Drugs 9:109-123. doi: 10.3390/md9010109
92. Liu G-L, Li Y, Chi Z, Chi Z-M (2011) Purification and characterization of κ-carrageenase from the marine bacterium Pseudoalteromonas porphyrae for hydrolysis of κ-carrageenan. Process Biochem 46:265-271. doi: 10.1016/j.procbio.2010.08.021
93. Liu Y, Lei Y, Zhang X, Gao Y, Xiao Y, Peng H (2012) Identification and phylogenetic characterization of a new subfamily of α-amylase enzymes from marine microorganisms. Mar Biotechnol (NY) 14:253-260. doi: 10.1007/s10126-011-9414-3
94. Liu Z, Li G, Mo Z, Mou H (2013) Molecular cloning, characterization, and heterologous expression of a new κ-carrageenase gene from marine bacterium Zobellia sp. ZM-2. Appl Microbiol Biotechnol 97:10057-10067. doi: 10.1007/s00253-013-5215-0
95. Longford S, Tujula N, Crocetti G, Holmes A, Holmström C, Kjelleberg S, Steinberg P, Taylor M (2007) Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquat Microb Ecol 48:217-229. doi: 10.3354/ame048217
96. Ma C, Lu X, Shi C, Li J, Gu Y, Ma Y, Chu Y, Han F, Gong Q, Yu W (2007) Molecular cloning and characterization of a novel beta-agarase, AgaB, from marine Pseudoalteromonas sp. CY24. J Biol Chem 282:3747-3754. doi: 10.1074/jbc.M607888200
97. Ma S, Duan G, Chai W, Geng C, Tan Y, Wang L, Le Sourd F, Michel G, Yu W, Han F (2013) Purification, cloning, characterization and essential amino acid residues analysis of a new ι-carrageenase from Cellulophaga sp. QY3. PLoS One 8:e64666
98. Mai Z, Yang J, Tian X, Li J, Zhang S (2013) Gene cloning and characterization of a novel salt-tolerant and glucose-enhanced β-glucosidase from a marine streptomycete. Appl Biochem Biotechnol 169:1512-1522
99. Malissard M, Duez C, Guinand M, Vacheron M-J, Michel G, Marty N, Joris B, Thamm I, Ghuysen J-M (1993) Sequence of a gene encoding a (poly ManA) alginate lyase acitve on Pseudomonas aeruginosa alginate. FEMS Microbiol Lett 110:101-106
100. Mayer AMS, Gustafson KR (2003) Marine pharmacology in 2000: antitumor and cytotoxic compounds. Int J Cancer 105:291-299. doi: 10.1002/ijc.11080
101. Mazure HG, Field JG (1980) Density and ecological importance of bacteria on kelp fronds in an upwelling region. J Exp Mar Biol Ecol 43:173-182
102. McHugh DJ (2003) A guide to the seaweed industry. FAO Fish Tech Pap 105
103. Meslet-Cladiere L, Delage L J-J, Leroux C, Goulitquer S, Leblanc C, Creis E, Gall E A, Stiger-Pouvreau V, Czjzek M, Potin P (2013) Structure/function analysis of a type III polyketide synthase in the brown alga Ectocarpus siliculosus reveals a biochemical pathway in phlorotannin monomer biosynthesis. Plant Cell 1-16. doi: 10.1105/tpc.113.111336
104. Meusnier I, Olsen JL, Stam WT, Destombe C, Valero M (2001) Phylogenetic analyses of Caulerpa taxifolia (Chlorophyta) and of its associated bacterial microflora provide clues to the origin of the Mediterranean introduction. Mol Ecol 10:931-946
105. Michel G, Czjzek M (2013) Polysaccharide-degrading enzymes from marine bacteria. In: Trincone A (ed) Marine enzymes for biocatalysis: sources, biocatalytic characteristic and bioprocesses of marine enzymes, Woodhead Publishing Series in Biomedicine, pp 429-464
106. Michel G, Chantalat L, Duee E, Barbeyron T, Henrissat B, Kloareg B, Dideberg O (2001a) 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
107. Michel G, Chantalat L, Fanchon E, Henrissat B, Kloareg B, Dideberg O (2001b) The iota-carrageenase of Alteromonas fortis. A beta-helix fold-containing enzyme for the degradation of a highly polyanionic polysaccharide. J Biol Chem 276:40202-40209. doi: 10.1074/jbc.M100670200
108. Michel G, Helbert W, Kahn R, Dideberg O, Kloareg B (2003) The structural bases of the processive degradation of ι-carrageenan, a main cell wall polysaccharide of red algae. J Mol Biol 334:421-433. doi: 10.1016/j.jmb.2003.09. 056
109. Michel G, Barbeyron T, Kloareg B, Czjzek M (2009) The family 6 carbohydrate-binding modules have coevolved with their appended catalytic modules toward similar substrate specificity. Glycobiology 19:615-623. doi: 10.1093/glycob/cwp028
110. Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010a) The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytol 188:82-97. doi: 10.1111/j.1469-8137.2010.03374.x
111. Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010b) Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus: insights into the origin and evolution of storage carbohydrates in Eukaryotes. New Phytol 188:67-81. doi: 10.1111/j.1469-8137.2010.03345.x
112. Mohapatra BR, Bapuji MAS (2003) Production of industrial enzymes (amylase, carboxymethylcellulase and protease) by bacteria isolated from marine sedentary organisms. Acta Biotechnol 23:75-84
113. Morris RM, Rappe MS, Connon SA, Vergin KL, Siebold WA, Carlson CA, Giovannoni SJ (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420:806-809. doi: 10.1038/nature01281.1
114. Nyvall Collén P, Sassi J-F, Rogniaux H, Marfaing H, Helbert W (2011) Ulvan lyases isolated from the Flavobacteria Persicivirga ulvanivorans are the first members of a new polysaccharide lyase family. J Biol Chem 286:42063-42071. doi: 10.1074/jbc.M111.271825
115. O'Sullivan L, Murphy B, McLoughlin P, Duggan P, Lawlor PG, Hughes H, Gardiner GE (2010) Prebiotics from marine macroalgae for human and animal health applications. Mar Drugs 8:2038-2064. doi: 10.3390/md8072038
116. Oh C, Nikapitiya C, Lee Y, Whang I, Kim S-J, Kang D-H, Lee J (2010) Cloning, purification and biochemical characterization of beta agarase from the marine bacterium Pseudoalteromonas sp. AG4. J Ind Microbiol Biotechnol 37:483-494. doi: 10.1007/s10295-010-0694-9
117. Ohta Y, Hatada Y (2006) A novel enzyme, lambda-carrageenase, isolated from a deep-sea bacterium. J Biochem 140:475-481
118. Pasmore M, Costerton JW (2003) Biofilms, bacterial signaling, and their ties to marine biology. J Ind Microbiol Biotechnol 30:407-413. doi: 10.1007/s10295-003-0069-6
119. Paul VJ, Puglisi MP (2004) Chemical mediation of interactions among marine organisms. Nat Prod Rep 21:189-209. doi: 10.1039/b302334f
120. Penesyan A, Marshall-Jones Z, Holmstrom C, Kjelleberg S, Egan S (2009) Antimicrobial activity observed among cultured marine epiphytic bacteria reflects their potential as a source of new drugs. FEMS Microbiol Ecol 69:113-124. doi: 10.1111/j.1574-6941.2009.00688.x
121. Pereira MS, Mulloy B, Mourao PAS (1999) Structure and anticoagulant activity of sulfated fucans: comparison between the regular, repetitive, and linear fucans from echinoderms with the more heteroheneous and branched polymers from brown algae. J Biol Chem 274:7656-7667. doi: 10.1074/jbc.274.12.7656
122. Pluvinage B, Hehemann J-H, Boraston AB (2013) Substrate recognition and hydrolysis by a family 50 exo-β-agarase, Aga50D, from the marine bacterium Saccharophagus degradans. J Biol Chem 288:28078-28088. doi: 10.1074/jbc.M113. 491068
123. Popper ZA, Michel G, Hervé C, Domozych DS, Willats WGT, Tuohy MG, Kloareg B, Stengel DB (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
124. Potin P, Richard C, Rochas C, Kloareg B (1993) Purification and characterization of the alpha-agarase from Alteromonas agarlyticus (Cataldi) comb. Nov., strain GJ1B. Eur J Biochem 214:599-607
125. Potin P, Bouarab K, Kupper F, Kloareg B (1999) Oligosaccharide recognition signals and defence reactions in marine plant-microbe interactions. Curr Opin Microbiol 2:276-283
126. Potin P, Bouarab K, Salaün J-P, Pohnert G, Kloareg B (2002) Biotic interactions of marine algae. Curr Opin Plant Biol 5:308-317. doi: 10.1016/S1369-5266(02)00273-X
127. Pushpamali WA, Nikapitiya C, De Zoysa M, Whang I, Kim SJ, Lee J (2008) Isolation and purification of an anticoagulant from fermented red seaweed Lomentaria catenata. Carbohydr Polym 73:274-279. doi: 10.1016/j.carbpol.2007.11. 029
128. Rajkumar R, Jayappriyan KR, Rengasamy R (2011) Purification and characterization of a protease produced by Bacillus megaterium RRM2: application in detergent and dehairing industries. J Basic Microbiol 51:614-624. doi: 10.1002/jobm.201000517
129. Rao TS (2010) Comparative effect of temperature on biofilm formation in natural and modified marine environment. Aquat Ecol 44:463-478. doi: 10.1007/s10452-009-9304-1
130. Read SM, Currie G, Bacic A (1996) Analysis of the structural heterogeneity of laminarin by electrospray-ionisation-mass spectrometry. Carbohydr Res 281:187-201
131. Rebuffet E, Barbeyron T, Jeudy A, Jam M, Czjzek M, Michel G (2010) Identification of catalytic residues and mechanistic analysis of family GH82 iota-carrageenases. Biochemistry 49:7590-7599. doi: 10.1021/bi1003475
132. Rebuffet E, Groisillier A, Thompson A, Jeudy A, Barbeyron T, Czjzek M, Michel G (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
133. Ren A, Xia Z-X, Yu W, Zhou J (2010) Expression, crystallization and preliminary X-ray analysis of an anomeric inverting agarase from Pseudoalteromonas sp. CY24. Acta Crystallogr Sect F: Struct Biol Cryst Commun 66:1635-1639. doi: 10.1107/S174430911004114X
134. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1-10. doi: 10.3354/meps243001
135. Salaün S (2009) Interactions entre la macroalgue brune Laminaria digitata et ses épibiontes bactériens: Etudes moléculaire et spectroscopiques, et capacité d ' adhésion et de formation de biofilm. Thesis, University of Pierre and Marie Curie, Paris, Fr
136. Salaün S, Kervarec N, Potin P, Haras D, Piotto M, La Barre S (2010) Whole-cell spectroscopy is a convenient tool to assist molecular identification of cultivatable marine bacteria and to investigate their adaptive metabolism. Talanta 80:1758-1770. doi: 10.1016/j.talanta.2009.10.020
137. Salaün S, La Barre S, Dos Santos-Goncalvez M, Potin P, Haras D, Bazire A (2012) Influence of exudates of the kelp Laminaria digitata on biofilm formation of associated and exogenous bacterial epiphytes. Microb Ecol 64:359-369. doi: 10.1007/s00248-012-0048-4
138. Sawabe T, Takahashi H, Ezura Y, Gacesa P (2001) Cloning, sequence analysis and expression of Pseudoalteromonas elyakovii IAM 14594 gene (alyPEEC) encoding the extracellular alginate lyase. Carbohydr Res 335:11-21
139. Schaumann K, Weide G (1995) Efficiency of uronic acid uptake in marine alginate-degrading fungi. Helgoländer Meeresuntersuchungen 49:159-167. doi: 10.1007/BF02368346
140. Schroeder DC (2003) Investigation of the role of a (1-4) agarase produced by Pseudoalteromonas gracilis B9 in eliciting disease symptoms in the red alga Gracilaria gracilis. Microbiology 149:2919-2929. doi: 10.1099/mic.0.26513-0
141. Staufenberger T, Thiel V, Wiese J, Imhoff JF (2008) Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiol Ecol 64:65-77. doi: 10.1111/j.1574-6941.2008.00445.x
142. Steinberg PD, de Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621-629
143. Stratil SB, Neulinger SC, Knecht H, Friedrichs AK, 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
144. Sugano Y, Matsumoto T, Kodama H, 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
145. Swanson PE (1999) Dehalogenases applied to industrial-scale biocatalysis. Curr Opin Biotechnol 10:365-369
146. Tait K, Williamson H, Atkinson S, Williams P, Cámara M, Joint I (2009) Turnover of quorum sensing signal molecules modulates cross-kingdom signalling. Environ Microbiol 11:1792-1802. doi: 10.1111/j.1462-2920.2009.01904. x
147. Takamatsu S, Hodges TW, Rajbhandari I, Gerwick WH, Hamann MT, Nagle DG (2003) Marine natural products as novel antioxidant prototypes. J Nat Prod 66:605-608. doi: 10.1021/np0204038
148. Taylor MW, Schupp PJ, Dahllöf I, Kjelleberg S, Steinberg PD (2003) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6:121-130. doi: 10.1046/j.1462-2920.2003.00545.x
149. Thomas F, Barbeyron T, Tonon T, Génicot S, Czjzek M, Michel G (2012) Characterization of the first alginolytic operons in a marine bacterium: from their emergence in marine Flavobacteriia to their independent transfers to marine Proteobacteria and human gut Bacteroides. Environ Microbiol 14:2379-2394. doi: 10.1111/j.1462-2920.2012.02751.x
150. Thomas F, Lundqvist LCE, Jam M, Jeudy A, Barbeyron T, Sandström C, Michel G, Czjzek M (2013) Comparative characterization of two marine alginate lyases from Zobellia galactanivorans reveals distinct modes of action and exquisite adaptation to their natural substrate. J Biol Chem 288:23021-23037. doi: 10.1074/jbc.M113.467217
151. Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42:117-126. doi: 10.1134/S0003683806020013
152. Tujula NA, Crocetti GR, Burke C, Thomas T, Holmström C, Kjelleberg S (2010) Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga. ISME J 4:301-311. doi: 10.1038/ismej.2009.107
153. Uchida M, Murata M (2004) Isolation of a lactic acid bacterium and yeast consortium from a fermented material of Ulva spp. (Chlorophyta). J Appl Microbiol 97:1297-1310. doi: 10.1111/j.1365-2672.2004.02425.x
154. Vera J, Castro J, Gonzalez A, Moenne A (2011) Seaweed polysaccharides and derived oligosaccharides stimulate defense responses and protection against pathogens in plants. Mar Drugs 9:2514-2525. doi: 10.3390/md9122514
155. Wargacki AJ, Leonard E, Win MN, Regitsky DD, Santos CNS, Kim PB, Cooper SR, Raisner RM, Herman A, Sivitz AB, Lakshmanaswamy A, Kashiyama Y, Baker D, Yoshikuni Y (2012) An engineered microbial platform for direct biofuel production from brown macroalgae. Science 335:308-313. doi: 10.1126/science. 1214547
156. Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9:2707-2719. doi: 10.1111/j.1462-2920. 2007.01383.x
157. Weinberger F, Friedlander M, Gunkel W (1994) A bacterial facultative parasite of Gracilaria conferta. Dis Aquat Org 18:135-141
158. Wiese J, Thiel V, Nagel K, Staufenberger T, Imhoff JF (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
159. Wilson GS, Raftos DA, Corrigan SL, Nair SV (2010) Diversity and antimicrobial activities of surface-attached marine bacteria from Sydney Harbour, Australia. Microbiol Res 165:300-311. doi: 10.1016/j.micres.2009.05.007
160. Wilson GS, Raftos DA, Nair SV (2011) Antimicrobial activity of surface attached marine bacteria in biofilms. Microbiol Res 166:437-448. doi: 10.1016/j.micres.2010.08.003
161. Yang J-I, Chen L-C, Shih Y-Y, Hsieh C, Chen C-Y, Chen W-M, Chen C-C (2011) Cloning and characterization of β-agarase AgaYT from Flammeovirga yaeyamensis strain YT. J Biosci Bioeng 112:225-232. doi: 10.1016/j.jbiosc.2011. 05.016
162. Yang J, Li J, Mai Z, Tian X, Zhang S (2013) Purification, characterization, and gene cloning of a cold-adapted thermolysin-like protease from Halobacillus sp. SCSIO 20089. J Biosci Bioeng 115:628-632. doi: 10.1016/j.jbiosc.2012.12.013
163. Yao Z, Wang F, Gao Z, Jin L, 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
164. Yaphe W (1957) The use of agarase from Pseudomonas atlantica in the identification of agar in marine algae (RHODOPHYCEAE). Can J Microbiol 3:987-993