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Differences of two polychaete species reflected in enzyme activities

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Abstract

Polychaetes constitute most of the benthic macroinvertebrates in estuarine and coastal environments. We investigated the utilization of organic matter in two polychaete species, Capitella sp. I and Perinereis nuntia brevicirris, living in different coastal habitats. The protease activity of Capitella sp. I (89.7 μg mg−1) was about 10 times that of P. nuntia brevicirris (8.0 μg mg−1). High cellulase (endo-β-1,4-glucanase) activity was detected in P. nuntia brevicirris (3.2 μg mg−1), whereas scarcely any was detected in Capitella sp. I. We isolated cDNA clones of protease mRNA from Capitella sp. I and of cellulase mRNA from P. nuntia brevicirris. The high protease activity of Capitella sp. I enabled it to survive in the sediment under a fish farm, where it degrades organic matter. In contrast, the high cellulase activity of the estuary-dwelling P. nuntia brevicirris allowed it to degrade organic matter originating from terrestrial areas.

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References

  • Antonio ES, Kasai A, Ueno M, Kurikawa Y, Tsuchiya K, Toyohara H, Ishihi Y, Yokoyama H, Yamashita Y (2010) Consumption of terrestrial organic matter by estuarine molluscs determined by analysis of their stable isotopes and cellulase activity. Estuar Coast Shelf Sci 86:401–407

    Article  CAS  Google Scholar 

  • Arnosti C, Ziervogel K, Ocampo L, Ghobrial S (2009) Enzyme activities in the water column and in shallow permeable sediments from the northeastern Gulf of Mexico. Estuar Coast Shelf Sci 84:202–208

    Article  CAS  Google Scholar 

  • Béguin P (1983) Detection of cellulase activity in polyacrylamide gels using Congo red-stained agar replicas. Anal Biochem 131:333–336

    Article  Google Scholar 

  • Byrne KA, Lehnert SA, Johnson SE, Moore SS (1999) Isolation of a cDNA encoding a putative cellulase in the red claw crayfish Cherax quadricarinatus. Gene 239:317–324

    Article  CAS  Google Scholar 

  • Chang S, Steimle FW, Reid RN, Fromm SA, Zdanowicz VS, Pikanowski RA (1992) Association of benthic macrofauna with habitat types and quality in the New York Bight. Mar Ecol Prog Ser 89:237–251

    Article  Google Scholar 

  • Chareonpanich C, Montani S, Tsutsumi H, Nakamura H (1994) Estimation of oxygen consumption of a deposit-feeding polychaete Capitella sp. I. Fish Sci 60:249–251

    Article  Google Scholar 

  • Davison A, Blaxter M (2005) Ancient origin of glycosyl hydrolase family 9 cellulase genes. Mol Biol Evol 22:1273–1284

    Article  CAS  Google Scholar 

  • Díaz-Mendoza M, Ortego F, García de Lacoba M, Magaña C, de la Poza M, Farinós GP, Castañera P, Hernández-Crespo P (2005) Diversity of trypsins in the Mediterranean corn borer Sesamia nonagrioides (Lepidoptera: Noctuidae), revealed by nucleic acid sequences and enzyme purification. Insect Biochem Mol Biol 35(9):1005–1020

    Article  Google Scholar 

  • Fu XY, Xue CH, Miao BC, Li ZJ, Gao X, Yang WG (2005) Characterization of proteases from the digestive tract of sea cucumber (Stichopus japonicus): high alkaline protease activity. Aquaculture 246:321–329

    Article  CAS  Google Scholar 

  • Halfon S, Craik C (1998) Trypsin. In: Barrett A, Rawlings N, Woessner J (eds) Handbook of proteolytic enzymes. Academic Press, London, pp 12–21

    Google Scholar 

  • Heilskov AC, Alperin M, Holmer A (2006) Benthic fauna bio-irrigation effects on nutrient regeneration in fish farm sediments. J Exp Mar Biol Ecol 339:204–225

    Article  Google Scholar 

  • Henriksen K, Rasmussen MB, Jensen A (1983) Effect of bioturbation on microbial nitrogen transformations in the sediment and fluxes of ammonium and nitrate to the overlaying water. Ecological Bull 35:193–205

    CAS  Google Scholar 

  • Hiroki M, Yabe T, Nohara S, Utagawa H, Satake K, Koga T, Ueno R, Kawachi M, Watanabe M (2003) Evaluation of an organic matter decomposing function from hydrolytic enzyme activities of tidal flat sediments in Japan. Jap J Limnol 64:113–120 (in Japanese)

    Article  CAS  Google Scholar 

  • Hu L, Guo Z, Feng J, Yanga Z, Fang M (2009) Distributions and sources of bulk organic matter and aliphatic hydrocarbons in surface sediments of the Bohai Sea, China. Mar Chem 113:197–211

    Article  CAS  Google Scholar 

  • Hutchings P (1998) Biodiversity and functioning of polychaetes in benthic sediments. Biodiversity Conserv 7:1133–1145

    Article  Google Scholar 

  • Johnston D, Moltschaniwskyj N, Wells J (2005) Development of the radula and digestive system of juvenile blacklip abalone (Haliotis rubra): potential factors responsible for variable weaning success on artificial diets. Aquaculture 250:341–355

    Article  Google Scholar 

  • Jorcin A (2000) Physical and chemical characteristics of the sediment in the estuarine region of Cananéia (SP), Brazil. Hydrobiologia 431:59–67

    Article  CAS  Google Scholar 

  • Jørgensen A, Rasmussen LJ, Andersen O (2005) Characterisation of two novel CYP4 genes from the marine polychaete Nereis virens and their involvement in pyrene hydroxylase activity. Biochem Biophys Res Commun 336:890–897

    Article  Google Scholar 

  • Kanaya G, Takagi S, Kikuchi E (2008) Spatial dietary variations in Laternula marilina (Bivalva) and Hediste spp. (Polychaeta) along environmental gradients in two brackish lagoons. Mar Ecol Prog Ser 359:133–144

    Article  CAS  Google Scholar 

  • Karakassis I, Tsapakis M, Hatziyanni E (1998) Seasonal variability in sediment profiles beneath fish farm cages in the Mediterranean. Mar Ecol Prog Ser 162:243–252

    Article  Google Scholar 

  • Karakassis I, Tsapakis M, Hatziyanni E, Papadopoulou K-N, Plaiti W (2000) Impact of cage farming of fish on the seabed in three Mediterranean coastal areas. ICES J Mar Sci 57:1462–1471

    Article  Google Scholar 

  • Kasai A, Nakata A (2005) Utilization of terrestrial organic matter by the bivalve Corbicula japonica estimated from stable isotope analysis. Fish Sci 71:151–158

    Article  CAS  Google Scholar 

  • Kashiwagi Y (2004) Enzymes of filamentous fungi in fermentation. MAFF Microorganism Genetic Resources Manual No 16:1–16

    Google Scholar 

  • Khademi S, Guarino LA, Watanabe H, Tokuda G, Meyer EF (2002) Structure of an endoglucanase from termite, Nasutitermes takasagoensis. Acta Cryst D 58:653–659

    Article  Google Scholar 

  • Kinoshita K, Tamaki S, Yoshioka M, Srithonguthai S, Kunihiro T, Hama D, Ohwada K, Tsutsumi H (2008) Bioremediation of organically enriched sediment deposited below fish farms with artificially mass-cultured colonies of a deposit-feeding polychaete Capitella sp. I. Fish Sci 74:77–87

    Article  CAS  Google Scholar 

  • Kunihiro T, Miyazaki T, Uramoto Y, Kinoshita K, Inoue A, Tamaki S, Hama D, Tsutsumi H, Ohwada K (2008) The succession of microbial community in the organic rich fish-farm sediment during bioremediation by introducing artificially mass-cultured colonies of a small polychaete, Capitella sp. I. Mar Pollut Bull 57:68–77

    Article  CAS  Google Scholar 

  • Li B, Bisgaard HC, Forbes VE (2004) Identification and expression of two novel cytochrome P450 genes, belonging to CYP4 and a new CYP331 family, in the polychaete Capitella capitata sp. I. Biochem Biophys Res Commun 325:510–517

    Article  CAS  Google Scholar 

  • Liccianoa M, Stabilia L, Giangrande A (2005) Clearance rates of Sabella spallanzanii and Branchiomma luctuosum (Annelida: Polychaeta) on a pure culture of Vibrio alginolyticus. Water Res 39:4375–4384

    Article  Google Scholar 

  • Llansó RJ (1991) Tolerance of low dissolved oxygen and hydrogen sulfide by the polychaete Streblospio benedicti (Webster). J Exp Mar Biol Ecol 153:165–178

    Article  Google Scholar 

  • Madin K, Sawasaki T, Ogasawara T, Endo Y (2000) A highly efficient and robust cell-free protein synthesis system prepared from wheat embryos: plants apparently contain a suicide system directed at ribosomes. Proc Natl Acad Sci USA 97:559–564

    Article  CAS  Google Scholar 

  • Main MB, Nelson WG (1988) Tolerance of the sabellariid polychaete Phragmatopoma lapidosa Kinberg to burial, turbidity and hydrogen sulfide. Mar Environ Res 26:39–56

    Article  CAS  Google Scholar 

  • Mazzola A, Mirto S, Rosa TL, Fabiano M, Danovaro R (2000) Fish-farming effects on benthic community structure in coastal sediments: analysis of meiofaunal recovery. ICES J Mar Sci 57:1454–1461

    Article  Google Scholar 

  • Michel C, Keil B (1975) Biologically active proteins in the venomous glands of the polychaetous annelid, Glycera convoluta Keferstein. Comp Biochem Physiol B Biochem Mol Biol 50:29–32

    Article  CAS  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Moens T, Luyten C, Middelburg JJ, Herman PMJ, Vincx M (2002) Tracing organic matter sources of estuarine tidal flat nematodes with stable carbon isotopes. Mar Ecol Prog Ser 234:127–137

    Article  Google Scholar 

  • Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6

    Article  CAS  Google Scholar 

  • Nishida Y, Suzuki K, Kumagai Y, Tanaka H, Inoue A, Ojima T (2007) Isolation and primary structure of a cellulase from the Japanese sea urchin Strongylocentrotus nudus. Biochimie 89:1002–1011

    Article  CAS  Google Scholar 

  • Nozaki M, Miura C, Tozawa Y, Miura T (2009) The contribution of endogenous cellulase to the cellulose digestion in the gut of earthworm (Pheretima hilgendorfi: Megascolecidae). Soil Biol Biochem 41:762–769

    Article  CAS  Google Scholar 

  • Papaspyrou S, Kristensen E, Christensen B (2007) Arenicola marina (Polychaeta) and organic matter mineralisation in sandy marine sediments: in situ and microcosm comparison. Estuar Coast Shelf Sci 72:213–222

    Article  Google Scholar 

  • Pawar V, Matsuda O, Yamamoto T, Hashimoto T, Rajendran N (2001) Spatial and temporal variations of sediment quality in and around fish cage farms: a case study of aquaculture in the Seto Inland Sea, Japan. Fish Sci 67:619–627

    Article  CAS  Google Scholar 

  • Peaucellier G (1983) Purification and characterization of proteases from the polychaete annelid Sabellaria alveolata (L.). Eur J Biochem 136:435–445

    Article  CAS  Google Scholar 

  • Riera P, Richard P (1996) Isotopic determination of food sources of Crassostrea gigas along a trophic gradient in the estuarine bay of Marennes-Oléron. Estuar Coast Shelf Sci 42:347–360

    Article  Google Scholar 

  • Rossi F (2002) Dynamics of the polychaetes Desdemona ornata and Perinereis cultrifera and their resources of food in a Mediterranean mudflat. Mar Ecol 23:285–296

    Article  Google Scholar 

  • Sakamoto K, Touhata K, Yamashita M, Kasai A, Toyohara H (2007) Cellulose digestion by common Japanese freshwater clam Corbicula japonica. Fish Sci 73:675–683

    Article  CAS  Google Scholar 

  • Sakamoto K, Uji S, Kurokawa T, Toyohara H (2008) Immunohistochemical, in situ hybridization and biochemical studies on endogenous cellulase of Corbicula japonica. Comp Biochem Physiol B Biochem Mol Biol 150:216–221

    Article  Google Scholar 

  • Sakon J, Irwin D, Wilson DB, Karplus PA (1997) Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca. Nat Struct Biol 4:810–818

    Article  CAS  Google Scholar 

  • Sawasaki T, Ogasawara T, Morishita R, Endo Y (2002) A cell-free protein synthesis system for high-throughput proteomics. Proc Natl Acad Sci USA 99:14652–14657

    Article  CAS  Google Scholar 

  • Smant G, Stokkermans JPWG, Yan Y, De Boer JM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J (1998) Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci USA 95:4906–4911

    Article  CAS  Google Scholar 

  • Sugimura M, Watanabe H, Lo N, Saito H (2003) Purification, characterization, cDNA cloning and nucleotide sequencing of a cellulase from the yellow-spotted longicorn beetle, Psacothea hilaris. Eur J Biochem 270:3455–3460

    Article  CAS  Google Scholar 

  • Suzuki K, Ojima T, Nishita K (2003) Purification and cDNA cloning of a cellulase from abalone Haliotis discus hannai. Eur J Biochem 270:771–778

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Tokuda G, Lo N, Watanabe H, Arakawa G, Matsumoto T, Noda H (2004) Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage. Mol Ecol 13:3219–3228

    Article  CAS  Google Scholar 

  • Tomassetti P, Persia E, Mercatali I, Vani D, Marussso V, Porrello S (2009) Effects of mariculture on macrobenthic assemblages in a western Mediterranean site. Mar Pollut Bull 58:533–541

    Article  CAS  Google Scholar 

  • Tomme P, Chauvaux S, Beguin P, Millet J, Aubert JP, Claeyssens M (1991) Identification of a histidyl residue in the active center of endoglucanase D from Clostridium thermocellum. J Biol Chem 266:10313–10318

    CAS  PubMed  Google Scholar 

  • Tomme P, van Beeumen J, Claeyssens M (1992) Modification of catalytically important carboxy residues in endoglucanase D from Clostridium thermocellum. Biochem J 285:319–324

    Article  CAS  Google Scholar 

  • Tsutsumi H (1990) Population persistence of Capitella sp. (Polychaeta; Capitellidae) on a mud flat subject to environmental disturbance by organic enrichment. Mar Ecol Prog Ser 63:147–156

    Article  Google Scholar 

  • Tsutsumi H, Montani S (1993) Utilization of biological activities of capitellid polychaete for treatment of “hedoro” (organically enriched sediment) deposited on the marine bottom below fish net pen culture. Nippon Suisan Gakkaishi 59:1343–1347 (in Japanese)

    Article  Google Scholar 

  • Tsutsumi H, Kinoshita K, Srithongouthai S, Sato A, Nagata S, Inoue A, Yoshioka M, Ohwada K, Hama D (2005) Treatment of the organically enriched sediment below a fish farm with the biological activities of artificially mass-cultured colonies of a small deposit feeding polychaete, Capitella sp. I. Benthos Res 60:25–38

    Article  Google Scholar 

  • Vezzulli L, Chelossi E, Riccardi G, Fabiano M (2002) Bacterial community structure and activity in fish farm sediments of the Ligurian Sea (western Mediterranean). Aquacult Int 10:123–141

    Article  CAS  Google Scholar 

  • Wada M, Zhang D, Do HK, Nishimura M, Tsutsumi H, Kogure K (2008) Co-inoculation of Capitella sp. I with its synergistic bacteria enhances degradation of organic matter in organically enriched sediment below fish farms. Mar Pollut Bull 57:86–93

    Article  CAS  Google Scholar 

  • Watanabe H, Tokuda G (2001) Animal cellulases. CMLS Cell Mol Life Sci 58:1167–1178

    Article  CAS  Google Scholar 

  • Watanabe H, Noda H, Tokuda G, Lo N (1998) A cellulase gene of termite origin. Nature 394:330–331

    Article  CAS  Google Scholar 

  • Xu B, Janson JC, Sellos D (2001) Cloning and sequencing of a molluscan endo-β-1, 4-glucanase gene from the blue mussel, Mytilus edulis. Eur J Biochem 268:3718–3727

    Article  CAS  Google Scholar 

  • Yokoyama H (2002) Impact of fish and pearl farming on the benthic environments in Gokasho Bay: evaluation from seasonal fluctuations of the macrobenthos. Fish Sci 68:258–268

    Article  CAS  Google Scholar 

  • Yokoyama H, Ishihi Y (2003) Feeding of the bivalve Theora lubrica on benthic microalgae: isotopic evidence. Mar Ecol Prog Ser 255:303–309

    Article  Google Scholar 

  • Yokoyama H, Abo K, Ishihi Y (2006) Quantifying aquaculture-derived organic matter in the sediment in and around a coastal fish farm using stable carbon and nitrogen isotope ratios. Aquaculture 25:411–425

    Article  Google Scholar 

  • Zhang L, Yin K, Wang L, Chen F, Zhang D, Yang Y (2009) The sources and accumulation rate of sedimentary organic matter in the Pearl River Estuary and adjacent coastal area, Southern China. Estuar Coast Shelf Sci 85:190–196

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Dr F. T. Celino (Ehime University) for critically reading the manuscript. We also thank Dr T. Kunihiro for collecting Capitella sp. I. This work was supported by the Global COE Program of the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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  1. South Ehime Fisheries Research Center, Ehime University, 1289-1, Funakoshi, Ainan, Ehime, 798-4292, Japan

    Katsutoshi Ito, Mana Nozaki, Chiemi Miura & Takeshi Miura

  2. Cell-Free Science and Technology Research Center and The Venture Business Laboratory, Ehime University, 3 Bunkyo-cho, Matsuyama, 790-8577, Japan

    Takashi Ohta & Yuzuru Tozawa

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  1. Katsutoshi Ito
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  2. Mana Nozaki
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  3. Takashi Ohta
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  6. Takeshi Miura
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Correspondence to Takeshi Miura.

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Communicated by H. O. Pörtner.

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Ito, K., Nozaki, M., Ohta, T. et al. Differences of two polychaete species reflected in enzyme activities. Mar Biol 158, 1211–1221 (2011). https://doi.org/10.1007/s00227-011-1641-7

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