Cite this paper:
Guangxun DU, Lingyun QU, Ping GAO, Wenhao HUANG, Chenghua LI, Dewen DING. Integration of metabolomics and transcriptomics revealed the biosynthetic mechanism of anti-parasitic compounds in Salinivibrio proteolyticus strain YCSC6[J]. Journal of Oceanology and Limnology, 2022, 40(1): 245-259

Integration of metabolomics and transcriptomics revealed the biosynthetic mechanism of anti-parasitic compounds in Salinivibrio proteolyticus strain YCSC6

Guangxun DU1,3, Lingyun QU2,3, Ping GAO2,3, Wenhao HUANG3, Chenghua LI1, Dewen DING1,3
1 School of Marine Sciences, Ningbo University, Ningbo 315832, China;
2 Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China;
3 Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources (MNR), Qingdao 266061, China
Abstract:
The fermentation broth of Salinivibrio proteolyticus strain YCSC6 shows potent anti-parasitic activity against Uronema marinum, with activity varying in each fermentation stage. To investigate the biosynthetic mechanism of anti-parasitic compounds in strain YCSC6, a comprehensive analysis of metabolomics and transcriptomics over four different time points (12, 24, 48, and 72 h) was performed. Metabolomics detected 17 943 metabolites with 1 129 known metabolites. A trend analysis of the known metabolites showed that 575 metabolites, including 69 polyketides, were continuously enhanced, being the potential source of anti-parasitic agents. In addition, 941 genes mapped to the same pathways of these metabolites, were screened through the association analysis of metabolites and genes. KEGG pathway enrichment of these genes showed 270 genes mapped to the biosynthesis of secondary metabolites and 192 genes mapped to the biosynthesis of antibiotics. This demonstrates the potent secondary metabolic capacity of strain YCSC6. Finally, a gene-metabolite correlation network was created based on the 575 continuously enhanced metabolites and 43 continuously up-regulated genes. This revealed 13 genes at the key position that mapped to a putative metabolic pathway associated with the biosynthesis of polyketides and caprylic acid, which contributes to the potent anti-parasitic activity of strain YCSC6. This comprehensive analysis of metabolomics and transcriptomics provides insights into the biosynthetic mechanisms of anti-parasitic compounds in strain YCSC6 and guides the exploitation of more anti-parasitic agents for aquaculture.
Key words:    metabolomics|transcriptomics|anti-parasitic|Salinivibrio proteolyticus|Uronema marinum   
Received: 2020-10-19   Revised:
Tools
PDF (2039 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Guangxun DU
Articles by Lingyun QU
Articles by Ping GAO
Articles by Wenhao HUANG
Articles by Chenghua LI
Articles by Dewen DING
References:
Anderson S A, Hulston D A, McVeagh S M, Webb V L, Smith P J. 2009. In vitro culture and cryopreservation of Uronema marinum isolated from farmed New Zealand groper (Polyprion oxygeneios). Journal of Microbiological Methods, 79(1): 62-66.
Bartel J, Krumsiek J, Schramm K, Adamski J, Gieger C, Herder C, Carstensen M, Peters A, Rathmann W, Roden M, Strauch K, Suhre K, Kastenmüller G, Prokisch H, Theis F J. 2015. The human blood metabolometranscriptome interface. PLoS Genetics, 11(6): e1005274.
Bender C L, Rangaswamy V, Loper J. 1999. Polyketide production by plant-associated pseudomonads. Annual Review of Phytopathology, 37: 175-196.
Cheung P J, Nigrelli R F, Ruggieri G D. 1980. Studies on the morphology of Uronema marinum Dujardin (Ciliatea: uronematidae) with a description of the histopathology of the infection in marine fishes. Journal of Fish Diseases, 3(4): 295-303.
Craster H L, Potter C A, Baumberg S. 1999. End-product control of expression of branched-chain amino acid biosynthesis genes in Streptomyces coelicolor A3(2): paradoxical relationships between DNA sequence and regulatory phenotype. Microbiology, 145(Pt 9): 2 375-2 384.
Csárdi G, Nepusz T. 2006. The igraph software package for complex network research. InterJournal Complex Systems. 1 695p.
Demarque D P, Dusi R G, de Sousa F D M, Grossi S M, Silvério M R S, Lopes N P, Espindola L S. 2020. Mass spectrometry-based metabolomics approach in the isolation of bioactive natural products. Scientific Reports, 10(1): 1 051.
Dourado M N, Bogas A C, Pomini A M, Andreote F D, Quecine M C, Marsaioli A J, Araújo W L. 2013. Methylobacterium-plant interaction genes regulated by plant exudate and quorum sensing molecules. Brazilian Journal of Microbiology, 44(4): 1 331-1 339.
Du G X, Qu L Y, Shang K, Gao P, Ding D W, Sun C J. 2020. Complete genome sequence of strain YCSC6, a marine bacterium isolated from saturated saltpan with activity against Uronema marinum. Current Microbiology, 77(1): 129-135.
Du G X, Qu L Y, Shang K, Sun C J, Wang C, Gao P. 2019. Ciliate Uronema marinum is the causative agent of scuticociliatosis in farm raised turbot Scophthalmus maximus. Journal of Oceanology and Limnology, 37(5): 1 726-1 735.
Du G X, Qu L Y, Shang K, Wang C, Gao P. 2017. Identification of marine bacterium YCSC6 and its insecticidal ability against Scuticociliate in vitro. Marine Sciences, 41(8): 24-31. (in Chinese with English abstract)
Duarte N, Kayser O, Abreu P, Ferreira M J U. 2008. Antileishmanial activity of piceatannol isolated from Euphorbia lagascae seeds. Phytotherapy Research, 22(4): 455-457.
Dyková I, Tyml T, Kostka M, Pecková H. 2010. Strains of Uronema marinum (Scuticociliatia) co-isolated with amoebae of the genus Neoparamoeba. Diseases of Aquatic Organisms, 89(1): 71-77.
Ernst J, Bar-Joseph Z. 2006. STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics, 7(1): 191.
Finney D J. 1971. Probit Analysis. 3rd edn. Cambridge University Press, Cambridge.
Geary T G, Jensen J B. 1983. Effects of antibiotics on Plasmodium falciparum in vitro. The American Journal of Tropical Medicine and Hygiene, 32(2): 221-225.
Harikrishnan R, Jin C N, Kim M C, Kim J S, Balasundaram C, Heo M S. 2010. Effectiveness and immunomodulation of chemotherapeutants against scuticociliate Philasterides dicentrarchi in olive flounder. Experimental Parasitology, 124(3): 306-314.
Harikrishnan R, Kim J S, Kim M C, Balasundaram C, Heo M S. 2011. Styrax japonica supplementation diet enhances the innate immune response in Epinephelus bruneus against bacterial and protozoan infections. Experimental Parasitology, 129(3): 260-265.
Hirazawa N, Oshima S I, Hata K. 2001. In vitro assessment of the antiparasitic effect of caprylic acid against several fish parasites. Aquaculture, 200(3-4): 251-258.
Hopwood D A, Sherman D H. 1990. Molecular genetics of polyketides and its comparison to fatty acid biosynthesis. Annual Review of Genetics, 24: 37-66.
Jee B Y, Kim Y C, Park M S. 2001. Morphology and biology of parasite responsible for scuticociliatosis of cultured olive flounder Paralichthys olivaceus. Diseases of Aquatic Organisms, 47(1): 49-55.
Jiang S P, Meadows J, Anderson S A, Mukkada A J. 2002. Antileishmanial activity of the antiulcer agent omeprazole. Antimicrobial Agents and Chemotherapy, 46(8): 2 569-2 574.
Jiménez C, Crews P. 1990. Novel marine sponge amino acids, 10. Xestoaminols from Xestospongia sp. Journal of Natural Products, 53(4): 978-982.
Kossuga M H, Nascimento A M, Reimão J Q, Tempone A G, Taniwaki N N, Veloso K, Ferreira A G, Cavalcanti B C, Pessoa C, Moraes M O, Mayer A M S, Hajdu E, Berlinck R G S. 2008. Antiparasitic, antineuroinflammatory, and cytotoxic polyketides from the marine sponge Plakortis angulospiculatus collected in Brazil. Journal of Natural Products, 71(3): 334-339.
Langmead B, Salzberg S L. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357-359.
Leite N F, Sobral-Souza C E, Albuquerque R S, Brito D I V, Lavor A K L S, Alencar L B B, Tintino S R, Ferreira J V A, Figueredo F G, Lima L F, Cunha F A B, Pinho A I, Coutinho H D M. 2013. In vitro cytotoxic and antiparasitic activity of caryophyllene and eugenol against Trypanosoma cruzi and Leishmania brasiliensis. Revista Cubana de Plantas Medicinales, 18(4): 522-528.
Li B, Dewey C N. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12(1): 323.
Liu Y M, Zhang Q Z, Xu D H, Fu Y W, Lin D J, Zhou S Y, Li J P. 2017. Antiparasitic efficacy of curcumin from Curcuma longa against Ichthyophthirius multifiliis in grass carp. Veterinary Parasitology, 236: 128-136.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods, 25(4): 402-408.
Marsden A F, Caffrey P, Aparicio J F, Loughran M S, Staunton J, Leadlay P F. 1994. Stereospecific acyl transfers on the erythromycin-producing polyketide synthase. Science, 263(5145): 378-380.
Mead J R, McNair N. 2006. Antiparasitic activity of flavonoids and isoflavones against Cryptosporidium parvum and Encephalitozoon intestinalis. FEMS Microbiology Letters, 259(1): 153-157.
Oden A, Wedel H. 1975. Arguments for fisher’s permutation test. Annals of Statistics, 3(2): 518-520.
Oldiges M, Lütz S, Pflug S, Schroer K, Stein N, Wiendahl C. 2007. Metabolomics: current state and evolving methodologies and tools. Applied Microbiology and Biotechnology, 76(3): 495-511.
Palmer-Young E C, Sadd B M, Stevenson P C, Irwin R E, Adler L S. 2016. Bumble bee parasite strains vary in resistance to phytochemicals. Scientific Reports, 6(1): 37087.
Perez-Souto N, Lynch R J, Measures G, Hann J T. 1992. Use of high-performance liquid chromatographic peak deconvolution and peak labelling to identify antiparasitic components in plant extracts. Journal of Chromatography A, 593(1-2): 209-215.
Sud M, Fahy E, Cotter D, Brown A, Dennis E A, Glass C K, MerrillJr A H, Murphy R C, Raetz C R H, Russell D W, Subramaniam S. 2007. LMSD: LIPID MAPS structure database. Nucleic Acids Research, 35(S1): D527-D532.
Sun X F, Huang X, Chen B, Li S P, He J. 2008. Isolation of a metsulfuron-methyl-resistant bacteria and cloning and expression of the acetohydroxyacid synthase genes ilvIH. Acta Microbiologica Sinica, 48(11): 1 493-1 498. (in Chinese with English abstract)
Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28(5): 511-515.
Wang G X, Han J, Zhao L W, Jiang D X, Liu Y T, Liu X L. 2010. Anthelmintic activity of steroidal saponins from Paris polyphylla. Phytomedicine, 17(14): 1 102-1 105.
Whang I, Kang H S, Lee J. 2013. Identification of scuticociliates (Pseudocohnilembus persalinus, P. longisetus, Uronema marinum and Miamiensis avidus) based on the cox1 sequence. Parasitology International, 62(1): 7-13.
Wishart D S, Jewison T, Guo A C, Wilson M, Knox C, Liu Y F, Djoumbou Y, Mandal R, Aziat F, Dong E, Bouatra S, Sinelnikov I, Arndt D, Xia J G, Liu P, Yallou F, Bjorndahl T, Perez-Pineiro R, Eisner R, Allen F, Neveu V, Greiner R, Scalbert A. 2013. HMDB 3.0—the human metabolome database in 2013. Nucleic Acids Research, 41(D1): D801-D807.
Yang K, Xia B R, Wang W J, Cheng J L, Yin M Z, Xie H Y, Li J N, Ma L B, Yang C Y, Li A, Fan X, Dhillon H S, Hou Y, Lou G, Li K. 2017. A comprehensive analysis of metabolomics and transcriptomics in cervical cancer. Scientific Reports, 7(1): 43353.
Yao J Y, Guo J L, Zang C S, Mi G Q, Jia Y Y, Yin W L, Cao Z, Xia Y C, Pan X Y, Ling L Y, Wang C F, Gu Z M, Shen J Y. 2019. Antiparasitic efficacy of natamycin isolated from Streptomyces gilvosporeu AXY-25 against Ichthyophthirius multifiliis. Aquaculture, 506: 465-469.
Yao J Y, Xu Y, Yin W L, Yuan X M, Lin L Y, Xu T, Zuo M L, Pan X Y, Shen J Y. 2015. Evaluation of nystatin isolated from Streptomyces griseus SDX-4 against the ciliate, Ichthyophthirius multifiliis. Parasitology Research, 114(4): 1 425-1 431.
Zhai Z H, Chen X N, Wang J. 2008. Primer design with primer premier 5.0. Northwest Medical Education, 16(4): 695-698. (in Chinese with English abstract)
Copyright © Haiyang Xuebao