Abstract
Sun-drying is a traditional process for preparing dried shrimp in coastal area of South China, but its impacts on nutrition and the formation of flavor-contributory substances in dried shrimp remain largely unknown. This study aimed to examine the effects of the production process on the microbiota and metabolites in dried shrimp. 16S rDNA amplicon sequencing was employed to identify 170 operational taxonomic units (OTUs), with Vibrio, Photobacterium, and Shewanella emerging as the primary pathogenic bacteria in shrimp samples. Lactococcus lactis was identified as the principal potential beneficial microorganism to accrue during the dried shrimp production process and found to contribute significantly to the development of desirable shrimp flavors. LC–MS-based analyses of dried shrimp sample metabolomes revealed a notable increase in compounds associated with unsaturated fatty acid biosynthesis, arachidonic acid metabolism, amino acid biosynthesis, and flavonoid and flavanol biosynthesis throughout the drying process. Subsequent exploration of the relationship between metabolites and bacterial communities highlighted the predominant coexistence of Bifidobacterium, Clostridium, and Photobacterium contributing heterocyclic compounds and metabolites of organic acids and their derivatives. Conversely, Arthrobacter and Staphylococcus were found to inhibit each other, primarily in the presence of heterocyclic compounds. This comprehensive investigation provides valuable insights into the dynamic changes in the microbiota and metabolites of dried shrimps spanning different drying periods, which we expect to contribute to enhancing production techniques and safety measures for dried shrimp processing.
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The original contributions presented in the study are available in SRA at https://www.ncbi.nlm.nih.gov/sra/PRJNA1041077.
References
Abedini E, Hajebzadeh H, Mirzai MA, Alahdadi AA (2022) Evaluation of operational parameters for drying shrimps in a cabinet hybrid dryer. Sol Energy 233:221–229. https://doi.org/10.1016/j.solener.2022.01.045
Akintola SL (2015) Effects of smoking and sun-drying on proximate, fatty and amino acids compositions of Southern pink shrimp (Penaeus notialis). J Food Sci Technol 52:2646–2656. https://doi.org/10.1007/s13197-014-1303-0
Akintola SL, Brown A, Bakare A, Osowo OD, Bello BO (2013) Effects of hot smoking and sun drying processes on nutritional composition of giant tiger shrimp (Penaeus monodon, Fabricius, 1798). Polish J food Nutr Sci 63:227–237. https://doi.org/10.2478/v10222-012-0093-1
Angelidis AS, Chronis EN, Papageorgiou DK, Kazakis II, Arsenoglou KC, Stathopoulos GA (2006) Non-lactic acid, contaminating microbial flora in ready-to-eat foods: a potential food-quality index. Food Microbiol 23:95–100. https://doi.org/10.1016/j.fm.2005.01.015
Bahrndorff S, Menanteau-Ledouble S, Stidsborg S, Jørgensen NOG, Hoque MS, Nielsen JL (2022) Bacterial composition associated with different traditions of salted and dried fish across countries. Food Biosci 50:101991. https://doi.org/10.1016/j.fbio.2022.101991
Beuchat LR, Ryu JH (1997) Produce handling and processing practices. Emerg Infect Dis 3:459–465. https://doi.org/10.3201/eid0304.970407
Biscola V, Todorov SD, Capuano VSC, Abriouel H, Gálvez A, Franco BDGM (2013) Isolation and characterization of a nisin-like bacteriocin produced by a Lactococcus lactis strain isolated from charqui, a Brazilian fermented, salted and dried meat product. Meat Sci 93:607–613. https://doi.org/10.1016/j.meatsci.2012.11.021
Burgess CM, Gianotti A, Gruzdev N, Holah J, Knøchel S, Lehner A, Margas E, Esser SS, Sela (Saldinger) S, Tresse O (2016) The response of foodborne pathogens to osmotic and desiccation stresses in the food chain. Int J Food Microbiol 221:37–53. https://doi.org/10.1016/j.ijfoodmicro.2015.12.014
Cerenius L, Söderhäll K (2021) Immune properties of invertebrate phenoloxidases. Dev Comp Immunol 122:104098. https://doi.org/10.1016/j.dci.2021.104098
Chambers MC, Maclean B, Burke R, Amodei D, Ruderman DL, Neumann S, Gatto L, Fischer B, Pratt B, Egertson J, Hoff K, Kessner D, Tasman N, Shulman N, Frewen B, Baker TA, Brusniak M-Y, Paulse C, Creasy D, Flashner L, Kani K, Moulding C, Seymour SL, Nuwaysir LM, Lefebvre B, Kuhlmann F, Roark J, Rainer P, Detlev S, Hemenway T, Huhmer A, Langridge J, Connolly B, Chadick T, Holly K, Eckels J, Deutsch EW, Moritz RL, Katz JE, Agus DB, MacCoss M, Tabb DL, Mallick P (2012) A cross-platform toolkit for mass spectrometry and proteomics. Nat Biotechnol 30:918–920. https://doi.org/10.1038/nbt.2377
Chen Q, Kong B, Han Q, Xia X, Xu L (2017) The role of bacterial fermentation in lipolysis and lipid oxidation in Harbin dry sausages and its flavour development. LWT 77:389–396. https://doi.org/10.1016/j.lwt.2016.11.075
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Chong J, Yamamoto M, Xia J (2019) MetaboAnalystR 2.0: from raw spectra to biological insights. metabolites 9:57. https://doi.org/10.3390/metabo9030057
Cornejo-Granados F, Lopez-Zavala AA, Gallardo-Becerra L, Mendoza-Vargas A, Sánchez F, Vichido R, Brieba LG, Viana MT, Sotelo-Mundo RR, Ochoa-Leyva A (2017) Microbiome of Pacific Whiteleg shrimp reveals differential bacterial community composition between Wild, Aquacultured and AHPND/EMS outbreak conditions. Sci Rep 7:11783. https://doi.org/10.1038/s41598-017-11805-w
Deng Y, Luo Y, Wang Y, Zhao Y (2015) Effect of different drying methods on the myosin structure, amino acid composition, protein digestibility and volatile profile of squid fillets. Food Chem 171:168–176. https://doi.org/10.1016/j.foodchem.2014.09.002
Derrickson-Tharrington E, Kendall PA, Sofos JN (2005) Inactivation of Escherichia coli O157:H7 during storage or drying of apple slices pretreated with acidic solutions. Int J Food Microbiol 99:79–89. https://doi.org/10.1016/j.ijfoodmicro.2004.07.015
Dolejš I, Rebroš M, Rosenberg M (2014) Immobilisation of Clostridium spp. for production of solvents and organic acids. Chem Pap 68:1–14. https://doi.org/10.2478/s11696-013-0414-9
Dou L, Chen W, Pan L, Huang F (2021) Characterization of Vibrio sp. strain AB15 and Pseudomonas fluorescens strain NB14 from the biofloc of shrimp culture ponds capable of high ammonia and nitrite removal efficiency. J World Aquaculture Soc 52:843–858. https://doi.org/10.1111/jwas.12789
Eckhardt TH, Skotnicka D, Kok J, Kuipers OP (2013) Transcriptional regulation of fatty acid biosynthesis in Lactococcus lactis. J Bacteriol 195:1081–1089. https://doi.org/10.1128/jb.02043-12
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
El Hage H, Herez A, Ramadan M, Bazzi H, Khaled M (2018) An investigation on solar drying: a review with economic and environmental assessment. Energy 157:815–829. https://doi.org/10.1016/j.energy.2018.05.197
Ernst J, Bar-Joseph Z (2006) STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 7:191. https://doi.org/10.1186/1471-2105-7-191
Faridnia F, Hussin ASM, Saari N, Mustafa S, Yee LY, Manap MYA (2010) In vitro binding of mutagenic heterocyclic aromatic amines by Bifidobacterium pseudocatenulatum G4. Benef Microbes 1:149–154. https://doi.org/10.3920/BM2009.0035
Flores M, Toldrá F (2011) Microbial enzymatic activities for improved fermented meats. Trends Food Sci Technol 22:81–90. https://doi.org/10.1016/j.tifs.2010.09.007
Grohmann U, Bronte V (2010) Control of immune response by amino acid metabolism. Immunol Rev 236:243–264. https://doi.org/10.1111/j.1600065X.2010.00915.x
Guo M, Wu F, Hao G, Qi Q, Li R, Li N, Wei L, Chai T (2017) Bacillus subtilis improves immunity and disease resistance in rabbits. Front Immunol 8:354. https://doi.org/10.3389/fimmu.2017.00354
Guo X, Xie C, Wang L, Li Q, Wang Y (2019) Biodegradation of persistent environmental pollutants by Arthrobacter sp. Environ Sci Pollut Res 26:8429–8443. https://doi.org/10.1007/s11356-019-04358-0
Ha AW, Kim WK (2018) Intake ratio and major food sources of n-3 and n-6 fatty acids in Korea: A study based on the sixth Korea national health and nutrition examination survey (2013–2014). Asia Pac J Clin Nutr 27:433–440. https://doi.org/10.3316/INFORMIT.568317014381821
Hernández Becerra JA, Ochoa Flores AA, Valerio-Alfaro G, Soto-Rodriguez I, Rodríguez-Estrada MT, García HS (2014) Cholesterol oxidation and astaxanthin degradation in shrimp during sun drying and storage. Food Chem 145:832–839. https://doi.org/10.1016/j.foodchem.2013.08.098
Hu Y, Zhang L, Liu Q, Wang Y, Chen Q, Kong B (2020) The potential correlation between bacterial diversity and the characteristic volatile flavour of traditional dry sausages from Northeast China. Food Microbiol 91:103505. https://doi.org/10.1016/j.fm.2020.103505
Huang X, Gu Y, Zhou H, Xu L, Cao H, Gai C (2020) Acinetobacter venetianus, a potential pathogen of red leg disease in freshwater-cultured whiteleg shrimp Penaeus vannamei. Aquaculture Reports 18:100543. https://doi.org/10.1016/j.aqrep.2020.100543
Huehn S, Eichhorn C, Urmersbach S, Breidenbach J, Bechlars S, Bier N, Alter T, Bartelt E, Frank C, Oberheitmann B, Gunzer F, Brennholt N, Böer S, Appel B, Dieckmann R, Strauch E (2014) Pathogenic vibrios in environmental, seafood and clinical sources in Germany. Int J Med Microbiol 304:843–850. https://doi.org/10.1016/j.ijmm.2014.07.010
Itay P, Shemesh E, Ofek-Lalzar M, Davidovich N, Kroin Y, Zrihan S, Stern N, Diamant A, Wosnick N, Meron D, Tchernov D, Morick D (2022) An insight into gill microbiome of Eastern Mediterranean wild fish by applying next generation sequencing. Front Mar Sci 9:1008103. https://doi.org/10.3389/fmars.2022.1008103
Joshi J, Srisala J, Truong VH, Chen I-T, Nuangsaeng B, Suthienkul O, Lo CF, Flegel TW, Sritunyalucksana K, Thitamadee S (2014) Variation in Vibrio parahaemolyticus isolates from a single Thai shrimp farm experiencing an outbreak of acute hepatopancreatic necrosis disease (AHPND). Aquaculture 428–429:297–302. https://doi.org/10.1016/j.aquaculture.2014.03.030
Kar A, Ghosh P, Patra P, Chini DS, Nath AK, Saha JK, Patra BC (2023) Omega-3 fatty acids mediated Cellular signaling and its regulation in Human Health. Clin Nutr Open Sci 20:72–86
Kleekayai T, Pinitklang S, Laohakunjit N, Suntornsuk W (2016) Volatile components and sensory characteristics of Thai traditional fermented shrimp pastes during fermentation periods. J Food Sci Technol 23:1399–1410. https://doi.org/10.1007/s13197-015-2142-3
Liao IC, Chien YH (2011) The Pacific white shrimp, Litopenaeus vannamei, in Asia: the world’s most widely cultured alien crustacean BT - In the wrong place - alien marine crustaceans: distribution, biology and impacts. In: Galil BS, Clark PF, Carlton JT (eds). Springer Netherlands, Dordrecht, pp 489–519. https://doi.org/10.1007/978-94-007-0591-3_17
Lin Y, Gao Y, Li A, Wang L, Ai Z, Xiao H, Li J, Li X (2022) Improvement of Pacific white shrimp (Litopenaeus vannamei) drying characteristics and quality attributes by a combination of salting pretreatment and microwave. Foods. https://doi.org/10.3390/foods11142066
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Neetoo H, Reega K, Manoga ZS, Nazurally N, Bhoyroo V, Allam M, Jaufeerally-Fakim Y, Ghoorah AW, Jaumdally W, Hossen AM, Mayghun F, Ismail A, Hosenally M (2022) Prevalence, genomic characterization, and risk assessment of human pathogenic vibrio species in seafood. J Food Prot 85:1553–1565. https://doi.org/10.4315/JFP-22-064
Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M (1999) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 27:29–34. https://doi.org/10.1093/nar/27.1.29
Oguzhan K, Hulya K, Hulagu B, Serefnur O (2022) Arachidonic acid metabolites in neurologic disorders. CNS Neurol Disord - Drug Targets 21:150–159. https://doi.org/10.2174/1871527320666210512013648
Oliver JD (2011) Chapter 18: culture media for the isolation and enumeration of pathogenic vibrio species in foods and environmental samples. Handbook of Culture Media for Food and Water Microbiology, pp 377–402. https://doi.org/10.1039/9781847551450-00377
Paudel A, Hamamoto H, Panthee S, Kaneko K, Matsunaga S, Kanai M, Suzuki Y, Sekimizu K (2017) A novel spiro-heterocyclic compound identified by the silkworm infection model inhibits transcription in Staphylococcus aureus. Front Microbiol 8:712. https://doi.org/10.3389/fmicb.2017.00712
Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. https://doi.org/10.1093/nar/gkm864
Roberts DW (2013) labdsv: ordination and multivariate analysis for ecology. R package version 2.0-1. https://CRAN.R-project.org/package=labdsv
Roshanak S, Rahimmalek M, Goli SAH (2016) Evaluation of seven different drying treatments in respect to total flavonoid, phenolic, vitamin C content, chlorophyll, antioxidant activity and color of green tea (Camellia sinensis or C. assamica) leaves. J Food Sci Technol 53:721–729. https://doi.org/10.1007/s13197-015-2030-x
Saelao S, Maneerat S, Kaewsuwan S, Rabesona H, Choiset Y, Haertlé T, Chobert J-M (2017) Inhibition of Staphylococcus aureus in vitro by bacteriocinogenic Lactococcus lactis KTH0-1S isolated from Thai fermented shrimp (Kung-som) and safety evaluation. Arch Microbiol 199:551–562. https://doi.org/10.1007/s00203-016-1324-3
Saelao S, Maneerat S, Thongruck K, Watthanasakphuban N, Wiriyagulopas S, Chobert J-M, Haertlé T (2018) Reduction of tyramine accumulation in Thai fermented shrimp (kung-som) by nisin Z-producing Lactococcus lactis KTH0–1S as starter culture. Food Control 90:249–258. https://doi.org/10.1016/j.foodcont.2018.03.003
Sampaio GR, Bastos DHM, Soares RAM, Queiroz YS, Torres EAFS (2006) Fatty acids and cholesterol oxidation in salted and dried shrimp. Food Chem 95:344–351. https://doi.org/10.1016/j.foodchem.2005.02.030
Sang X, Li K, Zhu Y, Ma X, Hao H, Bi J, Zhang G, Hou H (2020) The Impact of microbial diversity on biogenic amines formation in grasshopper sub shrimp paste during the fermentation. Front Microbiol 11:1–13. https://doi.org/10.3389/fmicb.2020.00782
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
Sikalidis AK (2015) Amino acids and immune response: a role for cysteine, glutamine, phenylalanine, tryptophan and arginine in t-cell function and cancer? Pathol Oncol Res 21:9–17. https://doi.org/10.1007/s12253-014-9860-0
Silvia G, Lorena N, Rogerio RS, Vito AC, Ana GC, Rosario GC, Luis AG, Luis DP, Eduardo GH, Karina DG, Alonso AL, Adrian O (2014) High-quality draft genomes of two Vibrio parahaemolyticus strains aid in understanding acute hepatopancreatic necrosis disease of cultured shrimps in Mexico. Genome Announc 2:e00800–14. https://doi.org/10.1128/genomea.00800-14
Sleator RD, Hill C (2002) Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26:49–71. https://doi.org/10.1111/j.1574-6976.2002.tb00598.x
Smith CA, Want EJ, O’Maille G, Abagyan R, Siuzdak G (2006) XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 78:779–787. https://doi.org/10.1021/ac051437y
Stevens MHH, Wagner H (2010) Vegan: community ecology package. R Packag Version 1:17–24
Stinson EE, Naftulin KA (1991) Effect of pH on organic acid production byClostridium propionicum in test tube and fermentor cultures. J Ind Microbiol 8:59–63. https://doi.org/10.1007/BF01575592
Stratakos AC, Koidis A (2015) Suitability, efficiency and microbiological safety of novel physical technologies for the processing of ready-to-eat meals, meats and pumpable products. Int J Food Sci Technol 50:1283–1302. https://doi.org/10.1111/ijfs.12781
Sun W, Ji H, Zhang D, Zhang Z, Liu S, Song W (2022) Evaluation of aroma characteristics of dried shrimp (Litopenaeus vannamei) prepared by five different procedures. Foods 11:3532. https://doi.org/10.3390/foods11213532
Toranzo AE, Magariños B, Avendaño-Herrera R (2017) Vibriosis: vibrio anguillarum, V. ordalii and Aliivibrio salmonicida. Fish Viruses and Bacteria: Pathobiology and Protection, pp 314–333. https://doi.org/10.1079/9781780647784.0314
Ward T, Larson J, Meulemans J, Hillmann B, Lynch J, Sidiropoulos D, Spear JR, Caporaso G, Blekhman R, Knight R, Fink R, Knights D (2017) BugBase predicts organism-level microbiome phenotypes. bioRxiv 133462. https://doi.org/10.1101/133462
Xia Z, Wu S (2018) Effects of glutathione on the survival, growth performance and non-specific immunity of white shrimps (Litopenaeus vannamei). Fish Shellfish Immunol 73:141–144. https://doi.org/10.1016/j.fsi.2017.12.015
Xu S, Li L, Tan Y, Feng J, Wei Z, Wang L (2000) Prediction and QSAR analysis of toxicity to Photobacterium phosphoreum for a group of heterocyclic nitrogen compounds. Bull Environ Contam Toxicol 64:316–322. https://doi.org/10.1007/s001280000002
Yu G, Wang L-G, Han Y, He Q-Y (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16:284–287. https://doi.org/10.1089/omi.2011.0118
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This work was supported by Funds for Guangdong University Innovation Team Project (2021KCXTD081), the Innovation Projects of Colleges and Universities in Guangdong Province (2019GKTSCX120), Basic and Applied Basic Research Foundation of Guangdong Province (2020A1515110332), and Foundation of Foshan Polytechnic (KY201902, KY201903).
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Conception and design of the work, MY and JL; analysis, MY, JL, JC, and MW; drafting the manuscript, MY, SD, and CL; editing and revising the manuscript, MY and JL. All authors have read and approved the final manuscript.
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Yu, M., Liu, J., Chen, J. et al. Metagenomic and metabolomic profiling of dried shrimp (Litopenaeus vannamei) prepared by a procedure traditional to the south China coastal area. Int Microbiol (2024). https://doi.org/10.1007/s10123-023-00475-6
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DOI: https://doi.org/10.1007/s10123-023-00475-6