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JIANG Yan, LIU Xuezhou, XU Yongjiang, SHI Bao, WANG Bin. Microbiota characteristics in Sebastes schlegelii intestine in early life stages[J]. HaiyangYuHuZhao, 2020, 38(1): 275-287

Microbiota characteristics in Sebastes schlegelii intestine in early life stages

JIANG Yan1,2, LIU Xuezhou1,2, XU Yongjiang1,2, SHI Bao1,2, WANG Bin1,2
1 Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China;
2 Laboratory for Marine Fisheries and Food Production Processes, Pilot National Laboratory for Marine Science and Technology(Qingdao), Qingdao 266237, China
The structure of intestinal microbiota of black rockfish Sebastes schlegelii in five early development stages were determined in high throughput sequencing with Illumina MiSeq PE300 system. The relationship between intestinal microbial community and the environmental (including culture water and feed) microbiota and the abundance variation trends of core microbiota were investigated, based on which the source of some core microbiota was analyzed in this study. The results show that Proteobacteria and Firmicutes are the most dominant phyla in guts. At the genus level, there are obvious differences between the artificial breeding fish and wild adults in the intestinal microflora structure. The compositions of dominant genera are similar, although the structure of intestinal microbiota gradually changes with the growth of larvae and juveniles. The core microbiota including Bacillus, Acinetobacter, Pseudomonas, Lactobacillus, Lactococcus, Glaciecola, Vibrio, Pseudoalteromonas, Acidovorax, and Aliivibrio were determined in the analysis of dominant and shared species. Compared with the water, the effect of feed microbiota on the structure of the gut microbial community is more obvious. Moreover, the trends of Bacillus, Acinetobacter, Pseudomonas, Lactobacillus, Lactococcus, and Glaciecola were opposite to Vibrio and Pseudoalteromonas in the gut. The correlation analysis suggested that Acidovorax, Glaciecola, Pseudomonas, Lactobacillus, and Acinetobacter might transited from mainly the parents and/or came from the fertilization process. The relative results may provide a theoretical reference for selecting the native probiotics, and supply the basic data for artificially regulating the intestinal microbiota with probiotic during early developmental stage of black rockfish.
Key words:    core microbiota|correlation analysis|intestinal microbiota|larva and juvenile|microbiota structure|Sebastes schlegelii   
Received: 2019-01-29   Revised:
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Adhikari M, Yadav D R, Kim S W, Um Y H, Kim H S, Lee S C, Song J Y, Kim H G, Lee Y S. 2017. Biological control of bacterial fruit blotch of watermelon pathogen(Acidovorax citrulli) with rhizosphere associated bacteria.Plant Pathology Journal, 33(2):170-183.
Alcaide E, Amaro C, Todoli R, Oltra R. 1999. Isolation and characterization of Vibrio parahaemolyticus causing infection in Iberian toothcarp Aphanius iberus. Diseases of Aquatic Organisms, 35(1):77-80.
Austin B, Zhang X H. 2006. Vibrio harveyi:a significant pathogen of marine vertebrates and invertebrates. Letters in Applied Microbiology, 43(2):119-124.
Baik K S, Park Y D, Seong C N, Kim E M, Bae K S, Chun J. 2006. Glaciecola nitratireducens sp. nov., isolated from seawater. International Journal of Systematic and Evolutionary Microbiology, 56(9):2 185-2 188.
Bakke I, Skjermo J, Vo T A, Vadstein O. 2013. Live feed is not a major determinant of the microbiota associated with cod larvae (Gadus morhua). Environmental Microbiology Reports, 5(4):537-548.
Banerjee G, Ray A K. 2017. Bacterial symbiosis in the fish gut and its role in health and metabolism. Symbiosis, 72(1):1-11,
Beurmann S, Ushijima B, Videau P, Svoboda C M, Smith A M, Rivers O S, Aeby G S, Callahan S M. 2017.Pseudoalteromonas piratica strain OCN003 is a coral pathogen that causes a switch from chronic to acute Montipora white syndrome in Montipora capitata. PLoS One, 12(11):e0188319.
Bolger A M, Lohse M, Usadel B. 2014. Trimmomatic:a flexible trimmer for Illumina sequence data.Bioinformatics, 30(15):2 114-2 120.
Chantharasophon K, Warong T, Mapatsa P, Leelavatcharamas V. 2011. High potential probiotic Bacillus species from gastro-intestinal tract of Nile Tilapia (Oreochromis niloticus). Biotechnology, 10(6):498-505.
Chen J G, Yang J F, Xiong J, Mao Z J, Wangh L. 2010. The innate immune response in Lateolabrax japonicus induced by lipopolysaccharide from Glaciecola polaris strain ARK149 (LMG21854). Agricultural Sciences in China, 9(10):1 504-1 511.
Chun S J, Cui Y S, Ko S R, Lee H G, Srivastava A, Oh H M, Ahn C Y. 2017. Acidovorax lacteus sp. nov., isolated from a culture of a bloom-forming cyanobacterium (Microcystis sp.). Antonie Van Leeuwenhoek, 110(9):1 199-1 205.
Chung H, Pamp S J, Hill J A, Surana N K, Edelman S M, Troy E B, Reading N C, Villablanca E J, Wang S, Mora J R, Umesaki Y, Mathis D, Benoist C, Relman D A, Kasper D L. 2012. Gut immune maturation depends on colonization with a host-specific microbiota. Cell, 149(7):1 578-1 593.
Dawood M A O, Koshio S. 2016. Recent advances in the role of probiotics and prebiotics in carp aquaculture:a review.Aquaculture, 454:243-251.
Desai A R, Links M G, Collins S A, Mansfield G S, Drew M D, Van Kessel A G, Hill J E. 2012. Effects of plant-based diets on the distal gut microbiome of rainbow trout(Oncorhynchus mykiss). Aquaculture, 350-353:134-142.
Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011.UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16):2 194-2 200.
Ferguson H W, Collins R O, Moore M, Coles M, MacPhee D D. 2004. Pseudomonas anguilliseptica infection in farmed cod, Gadus morhua L. Journal of Fish Disease, 27(4):249-253.
Ferreira C, Veldhoen M. 2012. Host and microbes date exclusively. Cell, 149(7):1 428-1 430.
Forsythe P, Bienenstock J. 2010. Immunomodulation by commensal and probiotic bacteria. Immunological Investigations, 39(4-5):429-448.
Gacias M, Gaspari S, Santos P M G, Tamburini S, Andrade M, Zhang F, Shen N, Tolstikov V, Kiebish M A, Dupree J L, Zachariou V, Clemente J C, Casaccia P. 2016. Microbiotadriven transcriptional changes in prefrontal cortex override genetic differences in social behavior. eLife, 5:e13442,
Gallo R L, Nakatsuji T. 2011. Microbial symbiosis with the innate immune defense system of the skin. Journal of Investigative Dermatology, 131(10):1 974-1 980.
Ghanbari M, Kneifel W, Domig K J. 2015. A new view of the fish gut microbiome:advances from next-generation sequencing. Aquaculture, 448:464-475.
Hjerde E, Lorentzen M S, Holden M T G, Seeger K, Paulsen S, Bason N, Churcher C, Harris D, Norbertczak H, Quail M A, Sanders S, Thurston S, Parkhill J, Willassen N P, Thomson N R. 2008. The genome sequence of the fish pathogen Aliivibrio salmonicida strain LFI1238 shows extensive evidence of gene decay. BMC Genomics, 9(1):616.
Horne M T, Baxendale A. 1983. The adhesion of Vibrio anguillarum to host tissues and its role in pathogenesis.Journal of Fish Diseases, 6(5):461-471.
Jiang Y, Liu Z X, Liu X Z, Xu Y J, Shi B, Wang B. 2019.Structural characteristics and succession of intestinal microbiota for Paralichthys olivaceus during the early life stage. Aquaculture Research, 50(2):529-540.
Jiang Y, Zhang Z, Wang Y G, Jing Y Y, Liao M J, Rong X J, Li B, Chen G P, Zhang H S. 2018. Effects of probiotic on microfloral structure of live feed used in larval breeding of turbot Scophthalmus maximus. Journal of Oceanology and Limnology, 36(3):1 002-1 012.
Karasov W H, Martínez del Rio C, Caviedes-Vidal E. 2011.Ecological physiology of diet and digestive systems.Annual Review of Physiology, 73:69-93.
Karlsen C, Vanberg C, Mikkelsen H, Sørum H. 2014. Coinfection of Atlantic salmon (Salmo salar), by Moritella viscosa and Aliivibrio wodanis, development of disease and host colonization. Veterinary Microbiology, 171(1-2):112-121.
Kelly P. 2010. Nutrition, intestinal defence and the microbiome.Proceedings of the Nutrition Society, 69(2):261-268.
Kim Y R, Kim E Y, Choi S Y, Hossain M T, Oh R K, Heo W S, Lee J M, Cho Y C, Kong I S. 2013. Effect of a probiotic strain, Enterococcus faecium, on the immune responses of olive flounder (Paralichthys olivaceus). Journal of Microbiology and Biotechnology, 22(4):526-529.
Kitani Y, Kikuchi N, Zhang G H, Ishizaki S, Shimakura K, Shiomi K, Nagashima Y. 2008. Antibacterial action of L-amino acid oxidase from the skin mucus of rockfish Sebastes schlegelii. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 149(2):394-400.
Kozińska A, Paździor E, Pękala A, Niemczuk W. 2014.Acinetobacter johnsonii and Acinetobacter lwoffii-the emerging fish pathogens. Bulletin of the Veterinary Institute in Pulawy, 58(2):193-199.
Leyton Y, Sayes C, Mejias C, Abarca M, Wilson R, Riquelme C. 2017. Increased larval survival of Seriola lalandi using Pseudoalteromonas sp. as probiotics. Revista de Biología Marina Y Oceanografía, 52(1):95-101.
Li J, Cao J L, Wang X, Liu N, Wang W M, Luo Y. 2017a.Acinetobacter pittii, an emerging new multi-drug resistant fish pathogen isolated from diseased blunt snout bream(Megalobrama amblycephala Yih) in China. Applied Microbiology and Biotechnology, 101(16):6 459-6 471.
Li X M, Yu Y H, Feng W S, Yan Q Y, Gong Y C. 2012. Host species as a strong determinant of the intestinal microbiota of fish larvae. Journal of Microbiology, 50(1):29-37.
Li Y X, Yang P, Zhang Y J, Ai Q H, Xu W, Zhang W B, Zhang Y A, Hu H B, Liu J T, Mai K S. 2017b. Effects of dietary glycinin on the growth performance, digestion, intestinal morphology and bacterial community of juvenile turbot, Scophthalmus maximus L. Aquaculture, 479:125-133.
Liu P C, Lin J Y, Hsiao P T, Lee K K. 2004. Isolation and characterization of pathogenic Vibrio alginolyticus from diseased cobia Rachycentron canadum. Journal of Basic Microbiology, 44(1):23-28.
Liu Y, Li N Q, Zhao X P, Yue B, He S W, Gao Z X, Zhou S, Zhang M. 2016. A C-type lectin that inhibits bacterial infection and facilitates viral invasion in black rockfish, Sebastes schlegelii. Fish & Shellfish Immunology, 57:309-317.
López-Romalde S, Magariños B, Nuñez S, Toranzo A E, Romalde J L. 2003. Phenotypic and genetic characterization of Pseudomonas anguilliseptica strains isolated from fish.Journal of Aquatic Animal Health, 15(1):39-47.
Lynch III J P, Zhanel G G, Clark N M. 2017. Infections due to Acinetobacter baumannii in the ICU:treatment Options.Seminars in Respiratory and Critical Care Medicine, 38(3):311-325.
Macpherson H L, Bergh Ø, Birkbeck T H. 2012. An aerolysinlike enterotoxin from Vibrio splendidus may be involved in intestinal tract damage and mortalities in turbot, Scophthalmus maximus (L.), and cod, Gadus morhua L., larvae. Journal of Fish Diseases, 35(2):153-167.
Magi G E, Lopez-Romalde S, Magariños B, Lamas J, Toranzo A E, Romalde J L. 2009. Experimental Pseudomonas anguilliseptica infection in turbot Psetta maxima (L.):a histopathological and immunohistochemical study.European Journal of Histochemistry, 53(2):e9.
Muñoz-Atienza E, Araújo C, Magadán S, Hernández P E, Herranz C, Santos Y, Cintas L M. 2014. In vitro and in vivo evaluation of lactic acid bacteria of aquatic origin as probiotics for turbot (Scophthalmus maximus L.) farming. Fish & Shellfish Immunology, 41(2):570-580.
Nicholson J K, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. 2012. Host-gut microbiota metabolic interactions. Science, 336(6086):1 262-1 267.
Nossa C W, Oberdorf W E, Yang L Y, Aas J A, Paster B J, DeSantis T Z, Brodie E L, Malamud D, Poles M A, Pei Z H. 2010. Design of 16S rRNA gene primers for 454 pyrosequencing of the human foregut microbiome. World Journal of Gastroenterology, 16(33):4 135-4 144.
Ntranos A, Casaccia P. 2018. The Microbiome-gut-behavior axis:crosstalk between the gut microbiome and oligodendrocytes modulates behavioral responses.Neurotherapeutics, 15(1):31-35.
Pérez T, Balcázar J L, Ruiz-Zarzuela I, Halaihel N, Vendrell D, de Blas I, Múzquiz J L. 2010. Host-microbiota interactions within the fish intestinal ecosystem. Mucosal Immunology, 3(4):355-360.
Pérez-Sánchez T, Ruiz-Zarzuela I, de Blas I, Balcázar J L. 2014. Probiotics in aquaculture:a current assessment.Reviews in Aquaculture, 6(3):133-146.
Qian G Y, Xu Z R. 2007. Effect of polysaccharide extracted from Glaciecola polaris on the protection of mouse macrophages from oxidative injury. Bioresource Technology, 98(1):202-206.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner F O. 2013. The SILVA ribosomal RNA gene database project:improved data processing and web-based tools. Nucleic Acids Research, 41(D1):D590-D596.
Reddy M R K, Mastan S A. 2013. Emerging Acinetobacter schindleri in red eye infection of Pangasius sutchi.African Journal of Biotechnology, 12(50):6 992-6 996.
Reyon D, Tsai S Q, Khayter C, Foden J A, Sander J D, Joung J K. 2012. FLASH assembly of TALENs for high-throughput genome editing. Nature Biotechnology, 30(5):460-465.
Richards G P, Watson M A, Needleman D S, Uknalis J, Boyd E F, Fay J P. 2017. Mechanisms for Pseudoalteromonas piscicida-induced killing of vibrios and other bacterial pathogens. Applied and Environmental Microbiology, 83(11):e00175,
Ringø E, Olsen R E, Mayhew T M, Myklebust R. 2003.Electron microscopy of the intestinal microflora of fish.Aquaculture, 227(1-4):395-415.
Rognes T, Flouri T, Nichols B, Quince C, Mahé F. 2016.VSEARCH:a versatile open source tool for metagenomics.PeerJ, 4:e2584.
Sanchez L M, Wong W R, Riener R M, Schulze C J, Linington R G. 2012. Examining the fish microbiome:vertebratederived bacteria as an environmental niche for the discovery of unique marine natural products. PLoS One, 7(5):e35398.
Shabat S K B, Sasson G, Doron-faigenboim A, Durman T, Yaacoby S, Berg Miller M E, White B A, Shterzer N, Mizrahi I. 2016. Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants. The ISME Journal, 10(12):2 958-2 972.
Smith P, Hiney M P, Samuelsen O B. 1994. Bacterial resistance to antimicrobial agents used in fish farming:a critical evaluation of method and meaning. Annual Review of Fish Diseases, 4:273-313.
Sullam K E, Essinger S D, Lozupone C A, O'Connor M P, Rosen G L, Knight R, Kilham S S, Russell J A. 2012.Environmental and ecological factors that shape the gut bacterial communities of fish:a meta-analysis. Molecular Ecology, 21(13):3 363-3 378.
Swain P, Nayak S K, Nanda P K, Dash S. 2008. Biological effects of bacterial lipopolysaccharide (endotoxin) in fish:a review. Fish & Shellfish Immunology, 25(3):191-201.
Tanaka S, Kobayashi T, Songjinda P, Tateyama A, Tsubouchi M, Kiyohara C, Shirakawa T, Sonomoto K, Nakayama J. 2009. Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. FEMS Immunology & Medical Microbiology, 56(1):80-87.
Urdaci M C, Bressollier P, Pinchuk I. 2004. Bacillus clausii probiotic strains:antimicrobial and immunomodulatory activities. Journal of Clinical Gastroenterology, 38(S6):S86-S90.
Verschuere L, Rombaut G, Sorgeloos P, Verstraete W. 2000.Probiotic bacteria as biological control agents in aquaculture. Microbiology and Molecular Biology Reviews, 64(4):655-671.
Wang Q, Garrity G M, Tiedje J M, Cole J R. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16):5 261-5 267.
Wong D, Nielsen T B, Bonomo R A, Pantapalangkoor P, Luna B, Spellberg B. 2017. Clinical and pathophysiological overview of Acinetobacter infections:a century of challenges. Clinical Microbiology Reviews, 30(1):409-447.
Yan L C, Hu B S, Chen G, Zhao M, Walcott R R. 2017. Further evidence of cucurbit host specificity among Acidovorax citrulli groups based on a detached melon fruit pathogenicity assay. Phytopathology, 107(11):1 305-1 311.
Ye L, Amberg J, Chapman D, Gaikowski M, Liu W T. 2014.Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish. The ISME Journal, 8(3):541-551.
Zhang Z G, Xu D M, Wang L, Hao J J, Wang J F, Zhou X, Wang W W, Qiu Q, Huang X D, Zhou J W, Long R J, Zhao F Q, Shi P. 2016. Convergent evolution of rumen microbiomes in high-altitude mammals. Current Biology, 26(14):1 873-1 879.
Zhao Y C, Yuan L, Wan J L, Sun Z X, Wang Y Y, Sun H S. 2016. Effects of potential probiotic Bacillus cereus EN25 on growth, immunity and disease resistance of juvenile sea cucumber Apostichopus japonicus. Fish & Shellfish Immunology, 49:237-242.
Ziaei-Nejad S, Rezaei M H, Takami G A, Lovett D L, Mirvaghefi A R, Shakouri M. 2006. The effect of Bacillus spp. bacteria used as probiotics on digestive enzyme activity, survival and growth in the Indian white shrimp Fenneropenaeus indicus. Aquaculture, 252(2-4):516-524.
Zorrilla I, Arijo S, Chabrillon M, Diaz P, Martinez-Manzanares E, Balebona M C, Moriñigo M A. 2003. Vibrio species isolated from diseased farmed sole, Solea senegalensis(Kaup), and evaluation of the potential virulence role of their extracellular products. Journal of Fish Diseases, 26(2):103-108.