Comparison of intestinal microbiota and activities of digestive and immune-related enzymes of sea cucumber <italic style="font-style: italic">Apostichopus japonicus</italic> in two habitats

Qi WANG; Xiumei ZHANG; Muyan CHEN; Wentao LI; Peidong ZHANG

doi:10.1007/s00343-018-7075-z

Your Location：

Home >

Browse articles >

Comparison of intestinal microbiota and activities of digestive and immune-related enzymes of sea cucumber Apostichopus japonicus in two habitats

Aquaculture and Fisheries | Updated：2023-05-19

- Comparison of intestinal microbiota and activities of digestive and immune-related enzymes of sea cucumber Apostichopus japonicus in two habitats
- Chinese Journal of Oceanology and Limnology Vol. 36, Issue 3, Pages: 990-1001(2018)
- Affiliations：
  
  1.Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao 266003, China
  2.Laboratory for Marine Fisheries and Aquaculture, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266072, China
- Author bio：
  
  ZHANG Xiumei, xiumei1227@163.com
- Funds：
- DOI：10.1007/s00343-018-7075-z
  CLC：
- Received：13 March 2017，
  
  Accepted：31 March 2017，
  
  Online First：09 May 2017，
  
  Published：2018-05
- Accepted：
Scan QR Code
Qi WANG, Xiumei ZHANG, Muyan CHEN, et al. Comparison of intestinal microbiota and activities of digestive and immune-related enzymes of sea cucumber Apostichopus japonicus in two habitats[J]. Chinese Journal of Oceanology and Limnology, 2018, 36(3): 990-1001.
DOI：

Qi WANG, Xiumei ZHANG, Muyan CHEN, et al. Comparison of intestinal microbiota and activities of digestive and immune-related enzymes of sea cucumber Apostichopus japonicus in two habitats[J]. Chinese Journal of Oceanology and Limnology, 2018, 36(3): 990-1001. DOI： 10.1007/s00343-018-7075-z.

摘要

Abstract

Sea cucumber

Apostichopus japonicus

stock enhancement by releasing hatchery-produced seeds is a management tool used to recover its population under natural environmental conditions. To assess the suitability of releasing sites

we examined the microbiota of the gut contents of

A. japonicus

from two populations (one in sandy-muddy seagrass beds and one in rocky intertidal reefs) and the microbiota in their surrounding sediments. The activities of digestive and immune-related enzymes in the

A. japonicus

were also examined. The results indicated that higher bacterial richness and Shannon diversity index were observed in all the seagrass-bed samples. There were significant differences in intestinal and sediment microorganisms between the two habitats

with a 2.87 times higher abundance of Firmicutes in the seagrass bed sediments than that in the reefs. Meanwhile

Bacteroidetes and Actinobacteria were significantly higher abundant in the gut content of

A. japonicus

from seagrass bed than those from the reefs. In addition

the seagrass-bed samples exhibited a relatively higher abundance of potential probiotics. Principal coordinates analysis and heatmap showed the bacterial communities were classified into two groups corresponding to the two habitat types. Moreover

compared to

A. japonicus

obtained from rocky intertidal habitat

those obtained from the seagrass bed showed higher lysozyme

superoxide dismutase and protease activities. Our results suggest that bacterial communities present in seagrass beds might enhance the digestive function and immunity of

A. japonicus

. Therefore

compared with the rocky intertidal reef

seagrass bed seems to be more beneficial for the survival of

A. japonicus

关键词

Keywords

references

Balcázar J L, de Blas I, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Múzquiz J L. 2006. The role of probiotics in aquaculture. Vet. Microbiol., 114(3-4):173-186.

Belcher P R, Consultant. 1997. Measurement of myocardial contractility. J. Cardiothorac. Vasc. Anesth., 11(6):812.

Bérdy J. 2005. Bioactive microbial metabolites:a personal view. J. Antibiot., 58(1):1-26.

Bordbar S, Anwar F, Saari N. 2011. High-value components and bioactives from sea cucumbers for functional foods-a review. Mar. Drugs, 9(10):1 761-1 805.

Bull A T, Stach J E M. 2007. Marine actinobacteria:new opportunities for natural product search and discovery.Trends Microbiol., 15(11):491-499.

Caporaso J G, Kuczynski J, Stombaugh J et al. 2010. QⅡME allows analysis of high-throughput community sequencing data. Nat. Methods, 7(5):335-336.

Chao A. 1984. Nonparametric estimation of the number of classes in a population. Scand. J. Stat., 11(4):265-270.

Cottrell M T, Kirchman D L. 2000. Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low-and high-molecularweight dissolved organic matter. Appl. Environ.Microbiol., 66(4):1 692-1 697.

Dou Y, Zhao X W, Ding J, He P. 2016. Application of highthroughput sequencing for analyzing bacterial communities in earthen ponds of sea cucumber aquaculture in northern China. Oceanol. Limnol. Sin., 47(1):122-129. (in Chinese with English abstract)

Dröge S, Limper U, Emtiazi F, Schönig I, Pavlus N, Drzyzga O, Fischer U, König H. 2005. In vitro and in vivo sulfate reduction in the gut contents of the termite Mastotermes darwiniensis and the rose-chafer Pachnoda marginata. J.Gen. Appl. Microbiol., 51(2):57-64.

Eliseikina M G, Magarlamov T Y. 2002. Coelomocyte Morphology in the Holothurians Apostichopus japonicus (Aspidochirota:Stichopodidae) and Cucumaria japonica (Dendrochirota:Cucumariidae). Russian Journal of Marine Biology, 28(3):197-202.

Fan Y, Li L, Yu X Q, Liu E F, Li T B, Xu L, Ye H B. 2015.Effect of Codonopsis pilosula as an immunopotentiator on intestinal bacterial community composition of Apostichopus japonicus. Chin. J. Anim. Nutrition, 27(2):638-646. (in Chinese with English abstract)

Gao F, Li F H, Tan J, Yan J P, Sun H L. 2014a. Bacterial community composition in the gut content and ambient sediment of sea cucumber Apostichopus japonicusrevealed by 16S rRNA gene pyrosequencing. PLoS One, 9(6):e100092, https://doi.org/10.1371/journal.pone.0100092.

Gao F, Sun H L, Xu Q, Tan J, Yan J P, Wang Q Y. 2010. PCRDGGE analysis of bacterial community composition in the gut contents of Apostichopus japonicus . J. Fish. Sci.China, 17(4):671-680. (in Chinese with English abstract)

Gao M L, Zhang G L, Hou H M. 2014b. Bacterial diversity in the intestine of Apostichopus japonicus in Dalian Bay. J.Dalian Polytech. Univ., 33(2):84-89. (in Chinese with English abstract)

Good I J. 1953. The population frequencies of species and the estimation of population parameters. Biometrika, 40(3-4):237-264.

Hassett R P, Landry M R. 1990. Seasonal changes in feeding rate, digestive enzyme activity, and assimilation efficiency of Calanus pacificus. Mar. Ecol. Prog. Ser., 62:203-210.

Jeon Y S, Park S C, Lim J, Chun J, Kim B S. 2015. Improved pipeline for reducing erroneous identification by 16S rRNA sequences using the Illumina MiSeq platform. J.Microbiol., 53(1):60-69.

Johnson P T. 1969.The coelomic elements of sea urchins( Strongylocentrotus ) Ⅲ. In vitro reaction to bacteria. J.Invertebr. Pathol., 13(1):42-54.

Jørgensen B B. 1982. Mineralization of organic matter in the sea bed-the role of sulphate reduction. Nature, 296(5858):643-645.

Jurasinski G, Retzer V, Beierkuhnlein C. 2009. Inventory, differentiation, and proportional diversity:a consistent terminology for quantifying species diversity. Oecologia, 159(1):15-26.

Li Q F, Zhang Y, Juck D, Fortin N, Greer C W, Tang Q S. 2010.Phylogenetic analysis of bacterial communities in the shrimp and sea cucumber aquaculture environment in northern China by culturing and PCR-DGGE. Aquacult.Int., 18(6):977-990.

Liu X J, Zhou Y, Yang H S, Ru S G. 2013. Eelgrass detritus as a food source for the sea cucumber Apostichopus japonicus selenka (echinidermata:holothuroidea) in coastal waters of North China:an experimental study in flow-through systems. PLoS One, 8(3):e58293, https://doi.org/10.1371/journal.pone.0058293.

Moriarty D J W. 1982. Feeding of Holothuria atra and Stichopus chloronotus on bacteria, organic carbon and organic nitrogen in sediments of the Great Barrier Reef.Mar. Freshw. Res., 33(2):255-263.

Muyzer G, de Waal E C, Uitterlinden A G. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of Polymerase Chain ReactionAmplified Genes Coding for 16S rRNA. Appl. Environ.Microbiol., 59(3):695-700.

O'Hara A M, Shanahan F. 2006. The gut flora as a forgotten organ. EMBO Reports, 7(7):688-693.

Pan K C, Yang H B. 1997. Progress in study of mechanism of Bacillus. Feed Ind., 18(9):32-34.

Peiffer J A, Spor A, Koren O, Jin Z, Tringe S G, Dangl J L, Buckler E S, Ley R E. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions.Proc. Natl. Acad. Sci. USA., 110(16):6 548-6 553.

Purcell S W, Hair C A, Mills D J. 2012. Sea cucumber culture, farming and sea ranching in the tropics:progress, problems and opportunities. Aquaculture, 368-369:68-81.

Rengpipat S, Rukpratanporn S, Piyatiratitivorakul S, Menasaveta P. 2000. Immunity enhancement in black tiger shrimp ( Penaeus monodon ) by a probiont bacterium( Bacillus S11). Aquaculture, 191(4):271-288.

Reyes-Bonilla H, Herrero-Pérezrul M D. 2003. Population parameters of an exploited population of Isostichopus fuscus (Holothuroidea) in the southern Gulf of California, México. Fisheries Research, 59(3):423-430.

Rosselló-Mora R, Amann R. 2001. The species concept for prokaryotes. FEMS Microbiol. Rev., 25(1):39-67.

Sögaard D H, Suhr-Jessen T. 1990. Microbials for feed beyond lactic acid bacteria. Feed Int., 11:32-38.

Sun Y, Chen D. 1989. The microbial composition of Stichopus japonicus and its physiological property. Oceanol.Limnol. Sin., 20(4):300-307. (in Chinese with English abstract)

Uthicke S. 2004. Over fishing of holothurians: lessons from the Great Barrier Reef. In : Lovatelli A, Conand C, Purcell S, Uthicke S, Hamel J F, Mercier A eds. Advances in Sea Cucumber Aquaculture and Management. Fao Report No. 463. FAO, Rome, p. 163-171.

Vaz-Moreira I, Egas C, Nunes O C, Manaia C M. 2011.Culture-dependent and culture-independent diversity surveys target different bacteria:a case study in a freshwater sample. Antonie van Leeuwenhoek, 100(2):245-257.

Verschuere L, Rombaut G, Sorgeloos P, Verstraete W. 2000.Probiotic bacteria as biological control agents in aquaculture. Microbiol. Mol. Biol. Rev., 64(4):655-671.

Wang J H, Zhao L Q, Liu J F, Wang H, Xiao S. 2015. Effect of potential probiotic Rhodotorula benthica D30 on the growth performance, digestive enzyme activity and immunity in juvenile sea cucumber Apostichopus japonicus . Fish Shellfish Immunol., 43(2):330-336.

Wang Y B, Li J R, Lin J. 2008. Probiotics in aquaculture:challenges and outlook. Aquaculture, 281(1-4):1-4.

Wu S G, Tian J Y, Gatesoupe F J, Li W X, Zou H, Yang B J, Wang T G. 2013. Intestinal microbiota of gibel carp( Carassius auratus gibelio ) and its origin as revealed by 454 pyrosequencing. World J. Microbiol. Biotechnol., 29(9):1 585-1 595.

Yuan C Y, Zhang H, Wu Y, Zhang L Y, Sun Y J. 2006. Effects of microecological preparation on growth and activities of digestive enzymes of sea cucumber Apostichopus japonicus . Fish. Sci., 25(12):612-615. (in Chinese with English abstract)

Zhang L B, Yang H S, Xu Q et al. 2011a. A new system for the culture and stock enhancement of sea cucumber, Apostichopus japonicus (Selenka), in cofferdams. Aquac.Res., 42(10):1 431-1 439.

Zhang P D, Sun Y, Niu S N, Zhang X M. 2011b. Research progress in seegrass seed dormancy, germination, and seedling growth and related affecting factors. Chin. J.Appl. Ecol., 22(11):3 060-3 066. (in Chinese with English abstract)

Zhang W J, Hou H M, Zhang G L, Li Q Y, Du C M. 2011c.Study on diversity of intestine cultivable microorganisms from Apostichopus japonicus. Sci. Technol. Food Ind., 32(9):149-151, 155. (in Chinese with English abstract)

Views

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

Diversity and community structure of eukaryotic microalgae in surface sediments in the central Bohai Sea, China, based on a metabarcoding approach

Transcriptome analysis of Porphyridium purpureum under salinities of 0 and 68

Physiological and histological responses of Phascolosoma esculenta (Sipuncula: Phascolosomatidea) to acute heat stress

Metabolomics analysis for skin ulceration syndrome ofApostichopus japonicusbased on UPLC/Q-TOF MS

Ultrastructural variation and key ER chaperones response induced by heat stress in intestinal cells of sea cucumber Apostichopus japonicus

Related Author

Tao JIANG

Lei LIU

Wencong ZHONG

Weiguo LI

Maoting WANG

Chaofan WANG

Zhaohui WANG

Qi LIU

Related Institution

School of Ocean, Yantai University

Engineering Research Center of Tropical and Subtropical Aquatic Ecological Engineering, Ministry of Education

College of Life Science and Technology, Jinan University

School of Life Science, Shanxi Key Laboratory for Research and Development of Regional Plants, Shanxi University

Ningbo Academy of Oceanology and Fisheries

Address：Editorial Office of JOL, 88 Haijun Rd. Qingdao, 266000, China
Tel：+86-532-82898754 Email：jol@qdio.ac.cn
Technical support is provided by Beijing Founder electronics co., LTD 京ICP备09064830号-19 京公网安备11010802024621
It is recommended to read the content of this site in Chrome&IE9+. Please switch to extreme mode in browser 360.
Cookies We use cookies to help provide and enhance our service and tailor content. By continuing, you agree to the use of cookies.

⁰

Comparison of intestinal microbiota and activities of digestive and immune-related enzymes of sea cucumber Apostichopus japonicus in two habitats

DOI：10.1007/s00343-018-7075-z

摘要

Abstract

关键词

Keywords

references