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Microbiota characteristics in Sebastes schlegelii intestine in early life stages

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Abstract

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.

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References

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Austin B, Zhang X H. 2006. Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Letters in Applied Microbiology, 43(2): 119–124.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Banerjee G, Ray A K. 2017. Bacterial symbiosis in the fish gut and its role in health and metabolism. Symbiosis, 72(1): 1–11, https://doi.org/10.1007/s13199-016-0441-8.

    Google Scholar 

  • 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.

    Google Scholar 

  • Bolger A M, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30(15): 2 114–2 120.

    Google Scholar 

  • 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.

    Google Scholar 

  • Chen J G, Yang J F, Xiong J, Mao Z J, Wangh L. 2010. The innate immune response in Lateolabraxjaponicus induced by lipopolysaccharide from Glaciecola polaris strain ARK149 (LMG21854). Agricultural Sciences in China, 9(10): 1 504–1 511.

    Google Scholar 

  • Chun S J, Cui Y S, Ko S R, Lee H G, Srivastava A, Oh H M, Ahn C Y. 2017. Acidovoraxlacteus sp. nov., isolated from a culture of a bloom-forming cyanobacterium (Microcystis sp.). Antonie Van Leeuwenhoek, 110(9): 1 199–1 205.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Ferreira C, Veldhoen M. 2012. Host and microbes date exclusively. Cell, 149(7): 1 428–1 430.

    Google Scholar 

  • Forsythe P, Bienenstock J. 2010. Immunomodulation by commensal and probiotic bacteria. Immunological Investigations, 39(4–5): 429–448.

    Google Scholar 

  • 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, https://doi.org/10.7554/eLife.13442.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Karlsen C, Vanberg C, Mikkelsen H, Serum H. 2014. Co-infection of Atlantic salmon (Salmo salar), by Moritella viscosa and Aliivibrio wodanis, development of disease and host colonization. Veterinary Microbiology, 171(1–2): 112–121.

    Google Scholar 

  • Kelly P. 2010. Nutrition, intestinal defence and the microbiome. Proceedings of the Nutrition Society, 69(2): 261–268.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Koziñska A, Pazdzior E, Pekala A, Niemczuk W. 2014. Acinetobacter johnsonii and Acinetobacter lwoffii-the emerging fish pathogens. Bulletin of the Veterinary Institute in Pulawy, 58(2): 193–199.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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, https://doi.org/10.1128/AEM.00175-17.

    Google Scholar 

  • 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.

    Google Scholar 

  • Rognes T, Flouri T, Nichols B, Quince C, Mahé F. 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ, 4: e2584.

    Google Scholar 

  • Sanchez L M, Wong W R, Riener R M, Schulze C J, Linington R G. 2012. Examining the fish microbiome: vertebrate-derived bacteria as an environmental niche for the discovery of unique marine natural products. PLoS One, 7(5): e35398.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Urdaci M C, Bressollier P, Pinchuk I. 2004. Bacillus clausii probiotic strains: antimicrobial and immunomodulatory activities. Journal of Clinical Gastroenterology, 38(S6): S86–S90.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

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  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

    Yan Jiang, Xuezhou Liu, Yongjiang Xu, Bao Shi & Bin Wang

  2. Laboratory for Marine Fisheries and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China

    Yan Jiang, Xuezhou Liu, Yongjiang Xu, Bao Shi & Bin Wang

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Correspondence to Xuezhou Liu.

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Supported by the Central Public-interest Scientific Institution Basal Research Fund, the CAFS and the Fund of Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, China (No. 2018HY-XKQ01-04), the Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (No. 2018SDKJ0501-2), the Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS, China (No. 20603022018021), the China Agriculture Research System (No. CARS-47), and the Key Project of Research and Development Plan of China (No. 2017YFE0104400)

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Jiang, Y., Liu, X., Xu, Y. et al. Microbiota characteristics in Sebastes schlegelii intestine in early life stages. J. Ocean. Limnol. 38, 275–287 (2020). https://doi.org/10.1007/s00343-019-9011-2

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