我国沿海典型水产养殖水域底泥中抗生素抗性细菌的多样性分析
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摘要
在水产养殖中,大量使用抗生素会改变水域中的菌落结构,并会诱导产生抗生素抗性菌,对养殖生物及人类健康构成潜在威胁。为初步掌握当前我国沿海养殖密集水域抗性菌的多样性概况,对我国沿海11个典型养殖区的底泥进行采样,选用常见的6种抗生素对菌株进行筛选,并基于Illumina MiSeq测序平台对抗性菌进行多样性分析。结果显示:1)不同养殖水域,其底泥中抗性菌的多样性存在一定的差异; 2)在大部分养殖水域,抗性菌属于变形菌门和厚壁菌门; 3)养殖水域底泥中细菌的多样性在不同抗生素的作用下差异显著。研究结果表明,海水养殖中使用抗生素对抗性菌多样性影响显著。研究结果有助于全面了解水产养殖活动对我国沿海典型养殖区抗性细菌多样性的影响,并可为抗生素使用的生态风险评估和应对策略提供参考。
In the process of aquaculture,the heavy use of antibiotics will change the bacterial structure in aquaculture waters,and will induce a large number of bacteria carrying antibiotic resistance genes,which is becoming a threat to the health of aquatic animals and human beings. In order to understand the biodiversity of antibiotic-resistant bacteria in the main intensive mariculture areas along the coastaline of China,this study selected 11 typical coastal aquaculture sites and sampled the substrate sludge. Two kinds of tetracyclines( tetracycline,oxytetracycline hydrochloride),two kinds of quinolones( ciprofloxacin,enrofloxacin),and two kinds of sulfonamides( sulfadiazine,sulfamethoxazole) were chosen to screen and characterize bacteria,respectively. IlluminaMiSeq high throughput sequencing platform was used to analyze the diversity of antibiotic-resistant bacteria. The results showed that:( 1) There is a significant difference in the diversity of antibiotic-resistant strains between different mariculture sites. The Chao index shows that the richness of anti-sulfamethoxazole bacterial communities is the highest and the richness of anti-enrofloxacin and ciprofloxacin bacterial communities are lower in most mariculture areas. In general,the richness of bacterial communities in the northern mariculture area is higher than that in the southern mariculture area. The Shannon index shows that in most mariculture areas,the diversity of bacterial communities in the sediment of antibiotics resistant to tetracycline and sulfonamide antibiotics are higher than the diversity of bacterial communities in the sediment of antibiotics resistant to quinolones,particularly among the highest diversity of bacterial communities resistant to sulfadiazine.( 2) In most aquaculture waters,antibiotic-resistant bacteria belong to Gammaproteobacteria and Firmicutes. In most of the waters, there are major advantages of Gammaproteobacteria,followed by the Firmicutes, and the advantage of Gammaproteobacteria in the mariculture area in the south is greater than that in the North Sea. In the sediments of most of the marine culture area,there are major advantages of Firmicutes,followed by the Gammaproteobacteria.( 3) The diversity of bacteria in aquaculture waters is significantly different under selective pressure of different antibiotics. The results showed that antibiotics used in mariculture significantly affected the diversity of antibiotic-resistant bacteria. The marine aquaculture has little effect on the bacteria in intensive aquaculture area on the level of phylum classification. But at the level of genus classification,the addition of different antibiotics can significantly change the diversity and richness of bacterial communities through the cluster analysis of each sample; with the addition of the same kind of antibiotics, the similarity of bacterial communities in adjacent waters is not high and there are great differences in the composition and structure of the bacterial community in the sediments from the northern and southern waters. The results could provide a basic data for understanding the effects of antibiotics on bacterial colonies in typical mariculture areas in the coastal waters of China,and provide reference information for ecological risk assessment and coping strategies of use of antibiotics.
In the process of aquaculture,the heavy use of antibiotics will change the bacterial structure in aquaculture waters,and will induce a large number of bacteria carrying antibiotic resistance genes,which is becoming a threat to the health of aquatic animals and human beings. In order to understand the biodiversity of antibiotic-resistant bacteria in the main intensive mariculture areas along the coastaline of China,this study selected 11 typical coastal aquaculture sites and sampled the substrate sludge. Two kinds of tetracyclines( tetracycline,oxytetracycline hydrochloride),two kinds of quinolones( ciprofloxacin,enrofloxacin),and two kinds of sulfonamides( sulfadiazine,sulfamethoxazole) were chosen to screen and characterize bacteria,respectively. IlluminaMiSeq high throughput sequencing platform was used to analyze the diversity of antibiotic-resistant bacteria. The results showed that:( 1) There is a significant difference in the diversity of antibiotic-resistant strains between different mariculture sites. The Chao index shows that the richness of anti-sulfamethoxazole bacterial communities is the highest and the richness of anti-enrofloxacin and ciprofloxacin bacterial communities are lower in most mariculture areas. In general,the richness of bacterial communities in the northern mariculture area is higher than that in the southern mariculture area. The Shannon index shows that in most mariculture areas,the diversity of bacterial communities in the sediment of antibiotics resistant to tetracycline and sulfonamide antibiotics are higher than the diversity of bacterial communities in the sediment of antibiotics resistant to quinolones,particularly among the highest diversity of bacterial communities resistant to sulfadiazine.( 2) In most aquaculture waters,antibiotic-resistant bacteria belong to Gammaproteobacteria and Firmicutes. In most of the waters, there are major advantages of Gammaproteobacteria,followed by the Firmicutes, and the advantage of Gammaproteobacteria in the mariculture area in the south is greater than that in the North Sea. In the sediments of most of the marine culture area,there are major advantages of Firmicutes,followed by the Gammaproteobacteria.( 3) The diversity of bacteria in aquaculture waters is significantly different under selective pressure of different antibiotics. The results showed that antibiotics used in mariculture significantly affected the diversity of antibiotic-resistant bacteria. The marine aquaculture has little effect on the bacteria in intensive aquaculture area on the level of phylum classification. But at the level of genus classification,the addition of different antibiotics can significantly change the diversity and richness of bacterial communities through the cluster analysis of each sample; with the addition of the same kind of antibiotics, the similarity of bacterial communities in adjacent waters is not high and there are great differences in the composition and structure of the bacterial community in the sediments from the northern and southern waters. The results could provide a basic data for understanding the effects of antibiotics on bacterial colonies in typical mariculture areas in the coastal waters of China,and provide reference information for ecological risk assessment and coping strategies of use of antibiotics.
引文
[1]农业部渔业局.中国渔业统计年鉴[M].北京:农业出版社,2014:23-52.Fishery Bureau, Ministry of Agriculture. China fishery statistics yearbook[M]. Beijing:Agriculture Press,2014:23-52.
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[4] RODRGUEZ-ROJAS A,RODRGUEZ-BELTRN J,COUCE A, et al. Antibiotics and antibiotic resistance:A bitter fight against evolution[J].International Journal of Medical Microbiology,2013,303:293-297.
[5] LEUNG K Y,SIAME B A,TENKINK B J,et al.Edwardsiella tarda—virulence mechanisms of an emerging gastroenteritis pathogen[J]. Microbes and Infection,2012,14(1):26-34.
[6] SHAH S Q A,KARATAS S,NILSEN H,et al.Characterization and expression of the gyr Agene from quinolone resistant Yersinia ruckeri strains isolated from Atlantic salmon(Salmo salar L.)in Norway[J]. Aquaculture,2012a,350-353:37-41.
[7]朱珣之,李强,李扬苹,等.紫茎泽兰入侵对土壤细菌的群落组成和多样性的影响[J].生物多样性,2015,23(5):665-672.ZHU X ZH,LI Q,LI Y P,et al. Eupatorium adenophorum invasion alters soil bacterial community and diversity[J]. Biodiversity Science,2015,23(5):665-672.
[8] EDGAR R C,HAAS B J,CLEMENTE J C,et al.CHIME improves sensitivity and speed of chimera detection[J]. Bioinformatics,2011,127(16):2194-2200.
[9] EDGAR R C. UPARSE:highly accurate OUT sequences from microbial ampliconreads[J]. Nature Methods,2013,10(10):996-998.
[10] WANG Q,GARRITY G M,TIDEJE J M,et al.Na6ve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy[J]. Applied and Environmrntal Microbiology,2007,73(16):5261-5267.
[11] DESANTIS T Z,HUGENHOLTZ P,LARSEN N,et al. Greengenes,a chimera-checked 16S rRNA gene database and workbench compatible with ARB[J].Applied and Environmrntal Microbiology,2006,72(7):5069-5072.
[12] CLASSEN A T,OVERBY S T,HART S C,et al.Season mediates herbivore effects on litter and soil microbial abundance and activity in a semi-arid woodland[J]. Plant and Soil,2007(295):217-227.
[13]张岱,杨吉顺,宋文武,等.盐碱土类型对花生种子萌发过程中种子际土壤菌群结构的影响[J].花生学报,2016,45(3):1-8.ZHANG D,YANG J S,SONG W W,et al. Effect of saline-alkali soil types on the microflora structure in the spermosphere during germination of peanut seeds[J]. Journal of Peanut Science,2016,45(3):1-8.
[14] ZHAO Z,WANG J,HAN Y,et al. Nutrients,heavy metals and microbial communities co-driven distribution of antibiotic resistance genes in adjacent environment of mariculture[J]. Environmental Pollution,2017,220(B):909-918.
[15] LIANG X,SHI Z,HUANG X. Occurrence of antibiotics in typical aquaculture ofthe Pearl River estuary[J].Ecology&Environmental Sciences,2013,22:304-310.
[16] HARNISZ M,KORZENIEWSKA E,GOLAS I. The impact of a freshwater fish farmon the community of tetracycline-resistant bacteria and the structure oftetracycline resistance genes in river water[J].Chemosphere,2015,128:134-141.
[17] CABELLO F C,GODFREY H P,TOMOVA A,et al. Antimicrobial use in aquaculture re-examined:its relevanceto antimicrobial resistance and to animal and human health[J]. Environmental Microbiology,2013,15:1917-1942.
[18]高盼盼,罗义,周启星,等.水产养殖环境中抗生素抗性基因(ARGS)的研究及进展[J].生态毒理学报,2009,4(6):770-779.GAO P P,LUO Y,ZHOU Q X,et al. Research advancement of antibiotics resistance genes(args)in aquaculture environment[J]. Asinan Journal of Ecotoxicolog,2009,4(6):770-779.
[19]李云莉,高权新,张晨捷,等.养殖水域抗生素抗性基因污染的研究概况与展望[J].海洋渔业,2017,39(3):351-360.LI Y Y,GAO Q X,ZHANG C J,et al. Current status and prospect ofantibiotic resistance genes(ARGs)pollution in the aquaculture[J]. Marine Fisheries,2017,39(3):351-360.
[20] DANG H,REN J,SONG L,et al. Diverse tetracycline resistant bacteria and resistance genes from coastal waters of Jiaozhou Bay[J]. Microbial Ecology,2008(55):237-246.
[21] DANG P K,DEGAND G,DANYI S,et al. Validation of a two-plate microbiological method for screening for screening antibiotic residues in shrimptissue[J].Marine Pollution Bulletin,2010(672):30-39.
[22] LOVE D C,RODMAN S,NEFF R A,et al.Veterinary drugresidues in seafood inspected by the European Union,United States,Canada,and Japan from 2000 to 2009[J]. Environmental Science&Technology,2011(45):7232-7240.
[23] AKINBOWALE O L,PENG H,BARTON M D.Antimicrobial resistance in bacteria isolated from aquaculture sources in Australia[J]. Journal of Applied Microbiology,2006(100):103-113.
[24] HARAKEH S,YASSINE H,HAJJAR S,et al.Isolates of Staphylococcus aureus and saprophyticus resistant to antimicrobials isolates from the Lebanese aquatic environment[J]. Marine Pollution Bulletin,2006(52):912-919.
[25] HOA P T P,NONAKA L,VIET P H,et al.Detection of the sul1, sul2, and sul3 genes insulfonamide-resistant bacteria from wastewater and shrimp ponds of north Vietnam[J]. Science of the Total Environment,2008(405):377-384.
[26] NONAKA L,IKENO K,SUZUKI S. Distribution of tetracycline gene, tet(M), in gram-positiveand gram-negative bacteria isolated from sediment and seawater at a coastal aquaculture site in Japan[J].Microbes and Environments,2007(22):355-364.
[27] KUMMERER K. Resistance in the environment[J].Journal of Antimicrobial Chemotherapy,2004(54):311-320.
[28] CAPLIN J L,HANLON G W,TAYLOR H D.Presence of vancomycin and ampicillin-resistant Enterococcus faecium of epidemic clonal complex-17in wastewaters from the south coast of England[J].Environmental Microbiology,2008(10):885-892.
[29] KIM S,AGA D S. Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants[J].Journal of Toxicology and Environmental Health(Part B),2007(10):559-573.
[30] SCHLUTER A,SZCZEPANOWSKI R,PUHLER A,et al. Genomics of Inc P-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for awidely accessible drug resistance gene pool[J]. Fems Microbiology Reviews,2007(31):449-77.
[31] SRUM H. Antibiotic resistance in aquaculture[J]. Acta Vet. Scand Suppl.,1999(92):29-36.
[32] LABELLA A,GENNARI M,GHIDINI V,et al.High incidence of antibiotic multi-resistant bacteria in coastal areas dedicated to fish farming[J].Marine Pollution Bulletin,2013,70(1-2):197-203.
[33] GAO P,MAO D,LUO Y,et al. Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment[J].Water Research. 2012,46(7):2355-2364.
[34] SHAH S Q,CABELLO F C,L’ABE-LUND T M,et al. Antimicrobial resistance and antimicrobial resistance genes in marine bacteria from salmon aquaculture and non-aquaculture sites[J].Environmental Microbiology,2014,16(5):1310-1320.
[35] NA G,ZHANG W,ZHOU S,et al. Sulfonamide antibiotics in the Northern Yellow Sea are related to resistant bacteria:implications for antibiotic resistance genes[J]. Marine Pollution Bulletin,2014,84(1-2):70-75.
[36] LI L,KATO C,HORIKOSHI K. Microbial diversity in sediments collected from the deepest cold-seep area,the Japan Trench[J]. Marine Biotechnology,1999(1):391-400.
[37] NAIR A V,VIJAYAN K K,CHAKRABORTY K,et al. Diversity and characterization of antagonistic bacteria from tropical estuarine habitats of Cochin,India for fish health management[J]. World Journal of Microbiology and Biotechnology,2012(28):2581-2592.
[38]窦妍,丁君,曲凌云,等.秋、冬季刺参养殖池塘菌群的多样性分析[J].大连海洋大学学报,2015,30(2):143-148.DOU Y,DING J,QU L Y,et al. Flora diversity in sea cucumber Apostichopus japonicus culture ponds in autumn and winter[J]. Journal of Dalian Fisheries University,2015,30(2):143-148.
[39]张翔,闫茂仓,肖国强,等.虾-贝-红树林耦合循环水养殖系统中微生物群落分析[J].水生生物学报,2016,40(3):557-564.ZHANG X,YAN M C,XIAO G Q,et al. Analysis of microbial community structure in mangrove constructed wetland-mariculture coupling system[J]. Acta Hydrobiologica Sinica,2016,40(3):557-564.
[40]黄宣运,沈晓盛,黄冬梅,等.室外池塘自然养殖条件下呋喃西林代谢物在中华绒螯蟹体内残留和消除规律[J].海洋渔业,2017,39(6)6:674-681.HUANG X Y,SHEN X S,HUANG D M,et al.Elimination rules of nitrofurazone metabolite residue in Eriocheir sinensis cultured in outdoor ponds[J].Marine Fisheries,2017,39(6):674-681.
[41]赵留杰,王元,常晓晴,等.盐酸氯苯胍药饵给药条件下在异育银鲫体内药动学和组织分布与消除规律[J].海洋渔业,2018,40(2):227-234.ZHAO L J, WANG Y, CHANG X Q, et al.Pharmacokinetics,tissue distribution and elimination of robenidine hydrochloride in Carassius auratus gibelio after oral administration via medicated feed[J]. Marine Fisheries,2018,40(2):227-234.
[2] Food and Agriculture Organization of the United Nation.FAO global aquaculture production volume and value satatistics database updated to 2012[DB]. Food and Agriculture Organization Fisheries and Aquaculture Department,2014.
[3]牛化欣,常杰.我国沿海滩涂水产养殖的发展现状与开发利用前景[J].科学养鱼,2011(10):4-5.NIU H X, CHANG J. Current situation and development prospect of aquaculture in coastal tidal flat in China[J]. Scientific Fish Farming,2011(10):4-5.
[4] RODRGUEZ-ROJAS A,RODRGUEZ-BELTRN J,COUCE A, et al. Antibiotics and antibiotic resistance:A bitter fight against evolution[J].International Journal of Medical Microbiology,2013,303:293-297.
[5] LEUNG K Y,SIAME B A,TENKINK B J,et al.Edwardsiella tarda—virulence mechanisms of an emerging gastroenteritis pathogen[J]. Microbes and Infection,2012,14(1):26-34.
[6] SHAH S Q A,KARATAS S,NILSEN H,et al.Characterization and expression of the gyr Agene from quinolone resistant Yersinia ruckeri strains isolated from Atlantic salmon(Salmo salar L.)in Norway[J]. Aquaculture,2012a,350-353:37-41.
[7]朱珣之,李强,李扬苹,等.紫茎泽兰入侵对土壤细菌的群落组成和多样性的影响[J].生物多样性,2015,23(5):665-672.ZHU X ZH,LI Q,LI Y P,et al. Eupatorium adenophorum invasion alters soil bacterial community and diversity[J]. Biodiversity Science,2015,23(5):665-672.
[8] EDGAR R C,HAAS B J,CLEMENTE J C,et al.CHIME improves sensitivity and speed of chimera detection[J]. Bioinformatics,2011,127(16):2194-2200.
[9] EDGAR R C. UPARSE:highly accurate OUT sequences from microbial ampliconreads[J]. Nature Methods,2013,10(10):996-998.
[10] WANG Q,GARRITY G M,TIDEJE J M,et al.Na6ve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy[J]. Applied and Environmrntal Microbiology,2007,73(16):5261-5267.
[11] DESANTIS T Z,HUGENHOLTZ P,LARSEN N,et al. Greengenes,a chimera-checked 16S rRNA gene database and workbench compatible with ARB[J].Applied and Environmrntal Microbiology,2006,72(7):5069-5072.
[12] CLASSEN A T,OVERBY S T,HART S C,et al.Season mediates herbivore effects on litter and soil microbial abundance and activity in a semi-arid woodland[J]. Plant and Soil,2007(295):217-227.
[13]张岱,杨吉顺,宋文武,等.盐碱土类型对花生种子萌发过程中种子际土壤菌群结构的影响[J].花生学报,2016,45(3):1-8.ZHANG D,YANG J S,SONG W W,et al. Effect of saline-alkali soil types on the microflora structure in the spermosphere during germination of peanut seeds[J]. Journal of Peanut Science,2016,45(3):1-8.
[14] ZHAO Z,WANG J,HAN Y,et al. Nutrients,heavy metals and microbial communities co-driven distribution of antibiotic resistance genes in adjacent environment of mariculture[J]. Environmental Pollution,2017,220(B):909-918.
[15] LIANG X,SHI Z,HUANG X. Occurrence of antibiotics in typical aquaculture ofthe Pearl River estuary[J].Ecology&Environmental Sciences,2013,22:304-310.
[16] HARNISZ M,KORZENIEWSKA E,GOLAS I. The impact of a freshwater fish farmon the community of tetracycline-resistant bacteria and the structure oftetracycline resistance genes in river water[J].Chemosphere,2015,128:134-141.
[17] CABELLO F C,GODFREY H P,TOMOVA A,et al. Antimicrobial use in aquaculture re-examined:its relevanceto antimicrobial resistance and to animal and human health[J]. Environmental Microbiology,2013,15:1917-1942.
[18]高盼盼,罗义,周启星,等.水产养殖环境中抗生素抗性基因(ARGS)的研究及进展[J].生态毒理学报,2009,4(6):770-779.GAO P P,LUO Y,ZHOU Q X,et al. Research advancement of antibiotics resistance genes(args)in aquaculture environment[J]. Asinan Journal of Ecotoxicolog,2009,4(6):770-779.
[19]李云莉,高权新,张晨捷,等.养殖水域抗生素抗性基因污染的研究概况与展望[J].海洋渔业,2017,39(3):351-360.LI Y Y,GAO Q X,ZHANG C J,et al. Current status and prospect ofantibiotic resistance genes(ARGs)pollution in the aquaculture[J]. Marine Fisheries,2017,39(3):351-360.
[20] DANG H,REN J,SONG L,et al. Diverse tetracycline resistant bacteria and resistance genes from coastal waters of Jiaozhou Bay[J]. Microbial Ecology,2008(55):237-246.
[21] DANG P K,DEGAND G,DANYI S,et al. Validation of a two-plate microbiological method for screening for screening antibiotic residues in shrimptissue[J].Marine Pollution Bulletin,2010(672):30-39.
[22] LOVE D C,RODMAN S,NEFF R A,et al.Veterinary drugresidues in seafood inspected by the European Union,United States,Canada,and Japan from 2000 to 2009[J]. Environmental Science&Technology,2011(45):7232-7240.
[23] AKINBOWALE O L,PENG H,BARTON M D.Antimicrobial resistance in bacteria isolated from aquaculture sources in Australia[J]. Journal of Applied Microbiology,2006(100):103-113.
[24] HARAKEH S,YASSINE H,HAJJAR S,et al.Isolates of Staphylococcus aureus and saprophyticus resistant to antimicrobials isolates from the Lebanese aquatic environment[J]. Marine Pollution Bulletin,2006(52):912-919.
[25] HOA P T P,NONAKA L,VIET P H,et al.Detection of the sul1, sul2, and sul3 genes insulfonamide-resistant bacteria from wastewater and shrimp ponds of north Vietnam[J]. Science of the Total Environment,2008(405):377-384.
[26] NONAKA L,IKENO K,SUZUKI S. Distribution of tetracycline gene, tet(M), in gram-positiveand gram-negative bacteria isolated from sediment and seawater at a coastal aquaculture site in Japan[J].Microbes and Environments,2007(22):355-364.
[27] KUMMERER K. Resistance in the environment[J].Journal of Antimicrobial Chemotherapy,2004(54):311-320.
[28] CAPLIN J L,HANLON G W,TAYLOR H D.Presence of vancomycin and ampicillin-resistant Enterococcus faecium of epidemic clonal complex-17in wastewaters from the south coast of England[J].Environmental Microbiology,2008(10):885-892.
[29] KIM S,AGA D S. Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants[J].Journal of Toxicology and Environmental Health(Part B),2007(10):559-573.
[30] SCHLUTER A,SZCZEPANOWSKI R,PUHLER A,et al. Genomics of Inc P-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for awidely accessible drug resistance gene pool[J]. Fems Microbiology Reviews,2007(31):449-77.
[31] SRUM H. Antibiotic resistance in aquaculture[J]. Acta Vet. Scand Suppl.,1999(92):29-36.
[32] LABELLA A,GENNARI M,GHIDINI V,et al.High incidence of antibiotic multi-resistant bacteria in coastal areas dedicated to fish farming[J].Marine Pollution Bulletin,2013,70(1-2):197-203.
[33] GAO P,MAO D,LUO Y,et al. Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment[J].Water Research. 2012,46(7):2355-2364.
[34] SHAH S Q,CABELLO F C,L’ABE-LUND T M,et al. Antimicrobial resistance and antimicrobial resistance genes in marine bacteria from salmon aquaculture and non-aquaculture sites[J].Environmental Microbiology,2014,16(5):1310-1320.
[35] NA G,ZHANG W,ZHOU S,et al. Sulfonamide antibiotics in the Northern Yellow Sea are related to resistant bacteria:implications for antibiotic resistance genes[J]. Marine Pollution Bulletin,2014,84(1-2):70-75.
[36] LI L,KATO C,HORIKOSHI K. Microbial diversity in sediments collected from the deepest cold-seep area,the Japan Trench[J]. Marine Biotechnology,1999(1):391-400.
[37] NAIR A V,VIJAYAN K K,CHAKRABORTY K,et al. Diversity and characterization of antagonistic bacteria from tropical estuarine habitats of Cochin,India for fish health management[J]. World Journal of Microbiology and Biotechnology,2012(28):2581-2592.
[38]窦妍,丁君,曲凌云,等.秋、冬季刺参养殖池塘菌群的多样性分析[J].大连海洋大学学报,2015,30(2):143-148.DOU Y,DING J,QU L Y,et al. Flora diversity in sea cucumber Apostichopus japonicus culture ponds in autumn and winter[J]. Journal of Dalian Fisheries University,2015,30(2):143-148.
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