Integration of metabolomics and transcriptomics revealed the biosynthetic mechanism of anti-parasitic compounds in <italic style="font-style: italic">Salinivibrio proteolyticus</italic> strain YCSC6

Guangxun DU; Lingyun QU; Ping GAO; Wenhao HUANG; Chenghua LI; Dewen DING

doi:10.1007/s00343-021-0466-6

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

Biology | Updated：2023-04-27

- Integration of metabolomics and transcriptomics revealed the biosynthetic mechanism of anti-parasitic compounds in Salinivibrio proteolyticus strain YCSC6
- Integration of metabolomics and transcriptomics revealed the biosynthetic mechanism of anti-parasitic compounds in Salinivibrio proteolyticus strain YCSC6
- 海洋湖沼学报（英文） 2022年40卷第1期页码：245-259
- Affiliations：
  
  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
- Author bio：
  
  Lingyun QU, E-mail: qly@fio.org.cn
- Funds：
  
  the National Key R & D Program of China(2017YFC1404504);the Youth Talent Program Supported by Laboratory for Marine Fisheries Science;Food Production Processes, Pilot National Laboratory for Marine Science and Technology(2018-MFS-T16);© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2022
- DOI：10.1007/s00343-021-0466-6
  中图分类号：
- 收稿：2020-10-19，
  
  录用：2020-11-24，
  
  网络首发：2021-02-10，
  
  纸质出版：2022-01
- Accepted：
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Integration of metabolomics and transcriptomics revealed the biosynthetic mechanism of anti-parasitic compounds in Salinivibrio proteolyticus strain YCSC6[J]. 海洋湖沼学报（英文）, 2022,40(1):245-259.

Guangxun DU, Lingyun QU, Ping GAO, et al. 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[J]. 海洋湖沼学报（英文）, 2022,40(1):245-259. DOI： 10.1007/s00343-021-0466-6.

Guangxun DU, Lingyun QU, Ping GAO, et al. 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. DOI： 10.1007/s00343-021-0466-6.

摘要

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

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.

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S A Anderson , D A Hulston , S M McVeagh , V L Webb , P J Smith . In vitro culture and cryopreservation of Uronema marinum isolated from farmed New Zealand groper ( Polyprion oxygeneios ) . Journal of Microbiological Methods , 2009 . 79 ( 1 ): 62 - 66 . DOI: 10.1016/j.mimet.2009.07.022 http://doi.org/10.1016/j.mimet.2009.07.022 .

J Bartel , J Krumsiek , K Schramm , J Adamski , C Gieger , C Herder , M Carstensen , A Peters , W Rathmann , M Roden , K Strauch , K Suhre , G Kastenmüller , H Prokisch , F J Theis . The human blood metabolometranscriptome interface . PLoS Genetics , 2015 . 11 ( 6 ): e1005274 DOI: 10.1371/journal.pgen.1005274 http://doi.org/10.1371/journal.pgen.1005274 .

C L Bender , V Rangaswamy , J Loper . Polyketide production by plant-associated pseudomonads . Annual Review of Phytopathology , 1999 . 37 175 - 196 . DOI: 10.1146/annurev.phyto.37.1.175 http://doi.org/10.1146/annurev.phyto.37.1.175 .

P J Cheung , R F Nigrelli , G D Ruggieri . 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 , 1980 . 3 ( 4 ): 295 - 303 . DOI: 10.1111/j.1365-2761.1980.tb00400.x http://doi.org/10.1111/j.1365-2761.1980.tb00400.x .

H L Craster , C A Potter , S Baumberg . 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 , 1999 . 145 ( Pt 9 ): 2 375 - 2 384 . .

Csárdi G, Nepusz T. 2006. The igraph software package for complex network research. InterJournal Complex Systems. 1695p.

D P Demarque , R G Dusi , F D M de Sousa , S M Grossi , M R S Silvério , N P Lopes , L S Espindola . Mass spectrometry-based metabolomics approach in the isolation of bioactive natural products . Scientific Reports , 2020 . 10 ( 1 ): 1 051 DOI: 10.1038/s41598-020-58046-y http://doi.org/10.1038/s41598-020-58046-y .

M N Dourado , A C Bogas , A M Pomini , F D Andreote , M C Quecine , A J Marsaioli , W L Araújo . Methylobacterium- plant interaction genes regulated by plant exudate and quorum sensing molecules . Brazilian Journal of Microbiology , 2013 . 44 ( 4 ): 1 331 - 1 339 . DOI: 10.1590/S1517-83822013000400044 http://doi.org/10.1590/S1517-83822013000400044 .

G X Du , L Y Qu , K Shang , P Gao , D W Ding , C J Sun . Complete genome sequence of strain YCSC6, a marine bacterium isolated from saturated saltpan with activity against Uronema marinum . Current Microbiology , 2020 . 77 ( 1 ): 129 - 135 . DOI: 10.1007/s00284-019-01796-4 http://doi.org/10.1007/s00284-019-01796-4 .

G X Du , L Y Qu , K Shang , C J Sun , C Wang , P Gao . Ciliate Uronema marinum is the causative agent of scuticociliatosis in farm raised turbot Scophthalmus maximus . Journal of Oceanology and Limnology , 2019 . 37 ( 5 ): 1 726 - 1 735 . DOI: 10.1007/s00343-020-8305-8 http://doi.org/10.1007/s00343-020-8305-8 http://www.jol343.com//EN/abstract/abstract813.shtml http://www.jol343.com//EN/abstract/abstract813.shtml , .

G X Du , L Y Qu , K Shang , C Wang , P Gao . Identification of marine bacterium YCSC6 and its insecticidal ability against Scuticociliate in vitro . Marine Sciences , 2017 . 41 ( 8 ): 24 - 31 . .

N Duarte , O Kayser , P Abreu , M J U Ferreira . Antileishmanial activity of piceatannol isolated from Euphorbia lagascae seeds . Phytotherapy Research , 2008 . 22 ( 4 ): 455 - 457 . DOI: 10.1002/ptr.2334 http://doi.org/10.1002/ptr.2334 .

I Dyková , T Tyml , M Kostka , H Pecková . Strains of Uronema marinum (Scuticociliatia) co-isolated with amoebae of the genus Neoparamoeba . Diseases of Aquatic Organisms , 2010 . 89 ( 1 ): 71 - 77 . .

J Ernst , Z Bar-Joseph . STEM: a tool for the analysis of short time series gene expression data . BMC Bioinformatics , 2006 . 7 ( 1 ): 191 DOI: 10.1186/1471-2105-7-191 http://doi.org/10.1186/1471-2105-7-191 .

D J Finney . Probit Analysis , 3 rd edn : Cambridge Cambridge University Press , 1971 .

T G Geary , J B Jensen . Effects of antibiotics on Plasmodium falciparum in vitro . The American Journal of Tropical Medicine and Hygiene , 1983 . 32 ( 2 ): 221 - 225 . DOI: 10.4269/ajtmh.1983.32.221 http://doi.org/10.4269/ajtmh.1983.32.221 .

R Harikrishnan , C N Jin , M C Kim , J S Kim , C Balasundaram , M S Heo . Effectiveness and immunomodulation of chemotherapeutants against scuticociliate Philasterides dicentrarchi in olive flounder . Experimental Parasitology , 2010 . 124 ( 3 ): 306 - 314 . DOI: 10.1016/j.exppara.2009.11.005 http://doi.org/10.1016/j.exppara.2009.11.005 .

R Harikrishnan , J S Kim , M C Kim , C Balasundaram , M S Heo . Styrax japonica supplementation diet enhances the innate immune response in Epinephelus bruneus against bacterial and protozoan infections . Experimental Parasitology , 2011 . 129 ( 3 ): 260 - 265 . DOI: 10.1016/j.exppara.2011.07.017 http://doi.org/10.1016/j.exppara.2011.07.017 .

N Hirazawa , S I Oshima , K Hata . In vitro assessment of the antiparasitic effect of caprylic acid against several fish parasites . Aquaculture , 2001 . 200 ( 3-4 ): 251 - 258 . DOI: 10.1016/S0044-8486(01)00529-4 http://doi.org/10.1016/S0044-8486(01)00529-4 .

D A Hopwood , D H Sherman . Molecular genetics of polyketides and its comparison to fatty acid biosynthesis . Annual Review of Genetics , 1990 . 24 37 - 66 . DOI: 10.1146/annurev.ge.24.120190.000345 http://doi.org/10.1146/annurev.ge.24.120190.000345 .

B Y Jee , Y C Kim , M S Park . Morphology and biology of parasite responsible for scuticociliatosis of cultured olive flounder Paralichthys olivaceus . Diseases of Aquatic Organisms , 2001 . 47 ( 1 ): 49 - 55 . .

S P Jiang , J Meadows , S A Anderson , A J Mukkada . Antileishmanial activity of the antiulcer agent omeprazole . Antimicrobial Agents and Chemotherapy , 2002 . 46 ( 8 ): 2 569 - 2 574 . DOI: 10.1128/AAC.46.8.2569-2574.2002 http://doi.org/10.1128/AAC.46.8.2569-2574.2002 .

C Jiménez , P Crews . Novel marine sponge amino acids, 10. Xestoaminols from Xestospongia sp . Journal of Natural Products , 1990 . 53 ( 4 ): 978 - 982 . DOI: 10.1021/np50070a033 http://doi.org/10.1021/np50070a033 .

M H Kossuga , A M Nascimento , J Q Reimão , A G Tempone , N N Taniwaki , K Veloso , A G Ferreira , B C Cavalcanti , C Pessoa , M O Moraes , A M S Mayer , E Hajdu , R G S Berlinck . Antiparasitic, antineuroinflammatory, and cytotoxic polyketides from the marine sponge Plakortis angulospiculatus collected in Brazil . Journal of Natural Products , 2008 . 71 ( 3 ): 334 - 339 . DOI: 10.1021/np0705256 http://doi.org/10.1021/np0705256 .

B Langmead , S L Salzberg . Fast gapped-read alignment with Bowtie 2 . Nature Methods , 2012 . 9 ( 4 ): 357 - 359 . DOI: 10.1038/nmeth.1923 http://doi.org/10.1038/nmeth.1923 .

N F Leite , C E Sobral-Souza , R S Albuquerque , D I V Brito , A K L S Lavor , L B B Alencar , S R Tintino , J V A Ferreira , F G Figueredo , L F Lima , F A B Cunha , A I Pinho , H D M Coutinho . In vitro cytotoxic and antiparasitic activity of caryophyllene and eugenol against Trypanosoma cruzi and Leishmania brasiliensis . Revista Cubana de Plantas Medicinales , 2013 . 18 ( 4 ): 522 - 528 . .

B Li , C N Dewey . RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome . BMC Bioinformatics , 2011 . 12 ( 1 ): 323 DOI: 10.1186/1471-2105-12-323 http://doi.org/10.1186/1471-2105-12-323 .

Y M Liu , Q Z Zhang , D H Xu , Y W Fu , D J Lin , S Y Zhou , J P Li . Antiparasitic efficacy of curcumin from Curcuma longa against Ichthyophthirius multifiliis in grass carp . Veterinary Parasitology , 2017 . 236 128 - 136 . DOI: 10.1016/j.vetpar.2017.02.011 http://doi.org/10.1016/j.vetpar.2017.02.011 .

K J Livak , T D Schmittgen . Analysis of relative gene expression data using real-time quantitative PCR and the 2 -ΔΔ C t method . Methods , 2001 . 25 ( 4 ): 402 - 408 . DOI: 10.1006/meth.2001.1262 http://doi.org/10.1006/meth.2001.1262 .

A F Marsden , P Caffrey , J F Aparicio , M S Loughran , J Staunton , P F Leadlay . Stereospecific acyl transfers on the erythromycin-producing polyketide synthase . Science , 1994 . 263 ( 5145 ): 378 - 380 . DOI: 10.1126/science.8278811 http://doi.org/10.1126/science.8278811 .

J R Mead , N McNair . Antiparasitic activity of flavonoids and isoflavones against Cryptosporidium parvum and Encephalitozoon intestinalis . FEMS Microbiology Letters , 2006 . 259 ( 1 ): 153 - 157 . DOI: 10.1111/j.1574-6968.2006.00263.x http://doi.org/10.1111/j.1574-6968.2006.00263.x .

A Oden , H Wedel . Arguments for fisher's permutation test . Annals of Statistics , 1975 . 3 ( 2 ): 518 - 520 . .

M Oldiges , S Lütz , S Pflug , K Schroer , N Stein , C Wiendahl . Metabolomics: current state and evolving methodologies and tools . Applied Microbiology and Biotechnology , 2007 . 76 ( 3 ): 495 - 511 . DOI: 10.1007/s00253-007-1029-2 http://doi.org/10.1007/s00253-007-1029-2 .

E C Palmer-Young , B M Sadd , P C Stevenson , R E Irwin , L S Adler . Bumble bee parasite strains vary in resistance to phytochemicals . Scientific Reports , 2016 . 6 ( 1 ): 37087 DOI: 10.1038/srep37087 http://doi.org/10.1038/srep37087 .

N Perez-Souto , R J Lynch , G Measures , J T Hann . Use of high-performance liquid chromatographic peak deconvolution and peak labelling to identify antiparasitic components in plant extracts . Journal of Chromatography A , 1992 . 593 ( 1-2 ): 209 - 215 . DOI: 10.1016/0021-9673(92)80288-6 http://doi.org/10.1016/0021-9673(92)80288-6 .

M Sud , E Fahy , D Cotter , A Brown , E A Dennis , C K Glass , A H MerrillJr , R C Murphy , C R H Raetz , D W Russell , S Subramaniam . LMSD: LIPID MAPS structure database . Nucleic Acids Research , 2007 . 35 ( S1 ): D527 - D532 . .

X F Sun , X Huang , B Chen , S P Li , J He . Isolation of a metsulfuron-methyl-resistant bacteria and cloning and expression of the acetohydroxyacid synthase genes ilv IH . Acta Microbiologica Sinica , 2008 . 48 ( 11 ): 1 493 - 1 498 . .

C Trapnell , B A Williams , G Pertea , A Mortazavi , G Kwan , M J van Baren , S L Salzberg , B J Wold , L Pachter . Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation . Nature Biotechnology , 2010 . 28 ( 5 ): 511 - 515 . DOI: 10.1038/nbt.1621 http://doi.org/10.1038/nbt.1621 .

G X Wang , J Han , L W Zhao , D X Jiang , Y T Liu , X L Liu . Anthelmintic activity of steroidal saponins from Paris polyphylla . Phytomedicine , 2010 . 17 ( 14 ): 1 102 - 1 105 . DOI: 10.1016/j.phymed.2010.04.012 http://doi.org/10.1016/j.phymed.2010.04.012 .

I Whang , H S Kang , J Lee . Identification of scuticociliates ( Pseudocohnilembus persalinus, P. longisetus, Uronema marinum and Miamiensis avidus ) based on the cox1 sequence . Parasitology International , 2013 . 62 ( 1 ): 7 - 13 . DOI: 10.1016/j.parint.2012.08.002 http://doi.org/10.1016/j.parint.2012.08.002 .

D S Wishart , T Jewison , A C Guo , M Wilson , C Knox , Y F Liu , Y Djoumbou , R Mandal , F Aziat , E Dong , S Bouatra , I Sinelnikov , D Arndt , J G Xia , P Liu , F Yallou , T Bjorndahl , R Perez-Pineiro , R Eisner , F Allen , V Neveu , R Greiner , A Scalbert . HMDB 3.0—the human metabolome database in 2013 . Nucleic Acids Research , 2013 . 41 ( D1 ): D801 - D807 . .

K Yang , B R Xia , W J Wang , J L Cheng , M Z Yin , H Y Xie , J N Li , L B Ma , C Y Yang , A Li , X Fan , H S Dhillon , Y Hou , G Lou , K Li . A comprehensive analysis of metabolomics and transcriptomics in cervical cancer . Scientific Reports , 2017 . 7 ( 1 ): 43353 DOI: 10.1038/srep43353 http://doi.org/10.1038/srep43353 .

J Y Yao , J L Guo , C S Zang , G Q Mi , Y Y Jia , W L Yin , Z Cao , Y C Xia , X Y Pan , L Y Ling , C F Wang , Z M Gu , J Y Shen . Antiparasitic efficacy of natamycin isolated from Streptomyces gilvosporeu AXY-25 against Ichthyophthirius multifiliis . Aquaculture , 2019 . 506 465 - 469 . DOI: 10.1016/j.aquaculture.2019.02.066 http://doi.org/10.1016/j.aquaculture.2019.02.066 .

J Y Yao , Y Xu , W L Yin , X M Yuan , L Y Lin , T Xu , M L Zuo , X Y Pan , J Y Shen . Evaluation of nystatin isolated from Streptomyces griseus SDX-4 against the ciliate, Ichthyophthirius multifiliis . Parasitology Research , 2015 . 114 ( 4 ): 1 425 - 1 431 . DOI: 10.1007/s00436-015-4325-2 http://doi.org/10.1007/s00436-015-4325-2 .

Z H Zhai , X N Chen , J Wang . Primer design with primer premier 5.0 . Northwest Medical Education , 2008 . 16 ( 4 ): 695 - 698 . .

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

DOI：10.1007/s00343-021-0466-6

摘要

Abstract

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