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http://dx.doi.org/10.4014/jmb.2011.11018

High Plasticity of the Gut Microbiome and Muscle Metabolome of Chinese Mitten Crab (Eriocheir sinensis) in Diverse Environments  

Chen, Xiaowen (School of Medicine, Tongji University)
Chen, Haihong (Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture/National Demonstration Center for Experimental Fisheries Science Education/Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University)
Liu, Qinghua (Fusuile Biotechnology Co., Ltd.)
Ni, Kangda (Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture/National Demonstration Center for Experimental Fisheries Science Education/Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University)
Ding, Rui (Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture/National Demonstration Center for Experimental Fisheries Science Education/Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University)
Wang, Jun (Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture/National Demonstration Center for Experimental Fisheries Science Education/Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University)
Wang, Chenghui (Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture/National Demonstration Center for Experimental Fisheries Science Education/Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University)
Publication Information
Journal of Microbiology and Biotechnology / v.31, no.2, 2021 , pp. 240-249 More about this Journal
Abstract
Phenotypic plasticity is a rapid response mechanism that enables organisms to acclimate and survive in changing environments. The Chinese mitten crab (Eriocheir sinensis) survives and thrives in different and even introduced habitats, thereby indicating its high phenotypic plasticity. However, the underpinnings of the high plasticity of E. sinensis have not been comprehensively investigated. In this study, we conducted an integrated gut microbiome and muscle metabolome analysis on E. sinensis collected from three different environments, namely, an artificial pond, Yangcheng Lake, and Yangtze River, to uncover the mechanism of its high phenotypic plasticity. Our study presents three divergent gut microbiotas and muscle metabolic profiles that corresponded to the three environments. The composition and diversity of the core gut microbiota (Proteobacteria, Bacteroidetes, Tenericutes, and Firmicutes) varied among the different environments while the metabolites associated with amino acids, fatty acids, and terpene compounds displayed significantly different concentration levels. The results revealed that the gut microbiome community and muscle metabolome were significantly affected by the habitat environments. Our findings indicate the high phenotypic plasticity in terms of gut microbiome and muscle metabolome of E. sinensis when it faces environmental changes, which would also facilitate its acclimation and adaptation to diverse and even introduced environments.
Keywords
Gut microbiome; metabolome; Eriocheir sinensis; phenotypic plasticity;
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1 Cheng Q, Zhou L, Wang C. 2013. Study on genetic variation and adaptive evolution from the native and colonized populations of Chinese mitten crab (in Chinese). J. Shanghai Ocean Univy. 22: 161-167.
2 Chen S, Zhou Y, Chen Y, Gu J. 2018. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34: i884-i890.   DOI
3 Magoc T, Salzberg SL. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27: 2957-2963.   DOI
4 Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998.   DOI
5 Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73: 5261-5267.   DOI
6 Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541.   DOI
7 Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Meth. 7: 335-336.   DOI
8 Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31: 814-821.   DOI
9 Wishart DS, Feunang YD, Marcu A, Guo AC, Liang K, Vazquez-Fresno R, et al. 2017. HMDB 4.0: the human metabolome database for 2018. Nucleic Acids Res. 46: D608-D617.   DOI
10 Thevenot EA, Roux A, Xu Y, Ezan E, Junot C. 2015. Analysis of the human adult urinary metabolome variations with age, body mass index, and gender by implementing a comprehensive workflow for univariate and OPLS statistical analyses. J. Proteome Res. 14: 3322-3335.   DOI
11 Chevalier C, Stojanovic O, Colin Didier J, Suarez-Zamorano N, Tarallo V, Veyrat-Durebex C, et al. 2015. Gut microbiota orchestrates energy homeostasis during cold. Cell 163: 1360-1374.   DOI
12 Alberdi A, Aizpurua O, Bohmann K, Zepeda-Mendoza ML, Gilbert MTP. 2016. Do vertebrate gut metagenomes confer rapid ecological adaptation? Trends Ecol. Evol. 31: 689-699.   DOI
13 Chen C-Y, Chen P-C, Weng FC-H, Shaw GT-W, Wang D. 2017. Habitat and indigenous gut microbes contribute to the plasticity of gut microbiome in oriental river prawn during rapid environmental change. PLoS One 12: e0181427.   DOI
14 Fox RJ, Donelson JM, Schunter C, Ravasi T, Gaitan-Espitia JD. 2019. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos. Trans. R Soc. Lond. B Biol. Sci. 374: 20180174.   DOI
15 Wang J, Gaughan S, Lamer JT, Deng C, Hu W, Wachholtz M, et al. 2020. Resolving the genetic paradox of invasions: preadapted genomes and postintroduction hybridization of bigheaded carps in the Mississippi River Basin. Evol. Appl. 13: 263-277.   DOI
16 Shin N-R, Whon TW, Bae J-W. 2015. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 33: 496-503.   DOI
17 Rothman JA, Leger L, Kirkwood JS, McFrederick QS. 2019. Cadmium and selenate exposure affects the honey bee microbiome and metabolome, and bee-associated bacteria show potential for bioaccumulation. Appl. Environ. Microbiol. 85: e01411-19.
18 Rudi K, Angell IL, Pope PB, Vik JO, Sandve SR, Snipen L-G. 2018. Stable core gut microbiota across the freshwater-to-saltwater transition for farmed Atlantic Salmon. Appl. Environ. Microbiol. 84: e01974-17.
19 Smith CCR, Snowberg LK, Gregory Caporaso J, Knight R, Bolnick DI. 2015. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. ISME J. 9: 2515-2526.   DOI
20 Gao Y-M, Zou K-S, Zhou L, Huang X-D, Li Y-Y, Gao X-Y, et al. 2020. Deep insights into gut microbiota in four carnivorous coral reef fishes from the South China Sea. Microorganisms 8: 426.   DOI
21 Liu H, Fu C, Ding G, Fang Y, Yun Y, Norra S. 2019. Effects of hairy crab breeding on drinking water quality in a shallow lake. Sci. Total Environ. 662: 48-56.   DOI
22 Chen L, Zhang Y, Liu Q, Hu Z, Sun Y, Peng Z, et al. 2015. Spatial variations of macrozoobenthos and sediment nutrients in Lake Yangcheng: Emphasis on effect of pen culture of Chinese mitten crab. J. Environ. Sci. 37: 118-129.   DOI
23 Naas AE, Mackenzie AK, Mravec J, Schuckel J, Willats WGT, Eijsink VGH, et al. 2014. Do rumen bcteroidetes utilize an alternative mechanism for cellulose degradation? mBio 5: e01401-14.
24 Smith JL, Boyer GL, Zimba PV. 2008. A review of cyanobacterial odorous and bioactive metabolites: Impacts and management alternatives in aquaculture. Aquaculture 280: 5-20.   DOI
25 Singh P, Teal TK, Marsh TL, Tiedje JM, Mosci R, Jernigan K, et al. 2015. Intestinal microbial communities associated with acute enteric infections and disease recovery. Microbiome 3: 45.   DOI
26 Li K, Dan Z, Gesang L, Wang H, Zhou Y, Du Y, et al. 2016. Comparative analysis of gut microbiota of native Tibetan and Han populations living at different altitudes. PLoS One 11: e0155863.   DOI
27 Chevin L-M, Lande R, Mace GM. 2010. Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory. PLoS Biol. 8: e1000357.   DOI
28 Malathi MV, Ravi PM, Anandham R, Gracy RG, Mohan M, Venkatesan T, et al. 2018. Gut bacterial diversity of insecticide-susceptible and -resistant nymphs of the brown planthopper Nilaparvata lugens stal (Hemiptera: Delphacidae) and elucidation of their putative functional roles. J. Microbiol. Biotechnol. 28: 976-986.   DOI
29 Sommer F, Stahlman M, Ilkayeva O, Arnemo JM, Kindberg J, Josefsson J, et al. 2016. The gut microbiota modulates energy metabolism in the hibernating brown bear Ursus arctos. Cell Rep. 14: 1655-1661.   DOI
30 Jarak I, Tavares L, Palma M, Rito J, Carvalho RA, Viegas I. 2018. Response to dietary carbohydrates in European seabass (Dicentrarchus labrax) muscle tissue as revealed by NMR-based metabolomics. Metabolomics 14: 95.   DOI
31 Lu J, Zhang X, Liu Y, Cao H, Han Q, Xie B, et al. 2019. Effect of fermented corn-soybean meal on serum immunity, the expression of genes related to gut immunity, gut microbiota, and bacterial metabolites in grower-finisher pigs. Front. Microbiol. 10: 2620.   DOI
32 Alvares TS, Conte CA, Paschoalin VM, Silva JT, Meirelles Cde M, Bhambhani YN, et al. 2012. Acute L-arginine supplementation increases muscle blood volume but not strength performance. Appl. Physiol. Nutr. Metab. 37: 115-126.   DOI
33 Martinez-Mota R, Kohl KD, Orr TJ, Denise Dearing M. 2019. Natural diets promote retention of the native gut microbiota in captive rodents. ISME J. 14: 67-78.   DOI
34 Sun Y, Han W, Liu J, Liu F, Cheng Y. 2020. Microbiota comparison in the intestine of juvenile Chinese mitten crab Eriocheir sinensis fed different diets. Aquaculture 515: 734518.   DOI
35 Tao H, Du B, Wang H, Dong H, Yu D, Ren L, et al. 2018. Intestinal microbiome affects the distinctive flavor of Chinese mitten crabs in commercial farms. Aquaculture 483: 38-45.   DOI
36 Kong L, Cai C, Ye Y, Chen D, Wu P, Li E, et al. 2012. Comparison of non-volatile compounds and sensory characteristics of Chinese mitten crabs (Eriocheir sinensis) reared in lakes and ponds: potential environmental factors. Aquaculture 364-365: 96-102.   DOI
37 Wang S, He Y, Wang Y, Tao N, Wu X, Wang X, et al. 2016. Comparison of flavour qualities of three sourced Eriocheir sinensis. Food Chem. 200: 24-31.   DOI
38 Saito Y, Yang Z, Hori K. 2001. The Huanghe (Yellow River) and Changjiang (Yangtze River) deltas: a review on their characteristics, evolution and sediment discharge during the Holocene. Geomorphology 41: 219-231.   DOI
39 Wang J, Xu P, Zhou G, Li X, Lu Q, Liu X, et al. 2018. Genetic improvement and breeding practices for Chinese mitten crab, Eriocheir sinensis. J. World Aquacult. Soc. 49: 292-301.   DOI
40 Buford TW, Kreider RB, Stout JR, Greenwood M, Campbell B, Spano M, et al. 2007. International society of sports nutrition position stand: creatine supplementation and exercise. J. Int. Soc. Sport Nutr. 4: 6.   DOI
41 Johnson CH, Ivanisevic J, Siuzdak G. 2016. Metabolomics: beyond biomarkers and towards mechanisms. Nat. Rev. Mol. Cell Biol. 17: 451.   DOI
42 Kakumanu ML, Maritz JM, Carlton JM, Schal C. 2018. Overlapping community compositions of gut and fecal microbiomes in lab-reared and field-collected German cockroaches. Appl. Environ. Microbiol. 84: e01037-01018.
43 Yang F, Zhao Ya E, Wei J-D, Lu Y-f, Zhang Y, Sun Y-l, et al. 2018. Comparison of microbial diversity and composition in jejunum and colon of the alcohol-dependent rats. J. Microbiol. Biotechnol. 28: 1883-1895.   DOI
44 Garcia A, Godzien J, Lopez-GonzalvezA, Barbas C. 2016. Capillary electrophoresis mass spectrometry as a tool for untargeted metabolomics. Bioanalysis 9: 99-130.   DOI
45 Hollywood K, Brison DR, Goodacre R. 2006. Metabolomics: current technologies and future trends. Proteomics 6: 4716-4723.   DOI
46 Herborg LM, Rushton SP, Clare AS, Bentley MG. 2005. The invasion of the Chinese mitten crab (Eriocheir sinensis) in the United Kingdom and its comparison to continental Europe. Biol. Invasions. 7: 959-968.   DOI
47 Wang W, Wang C, Ma X. 2013. Ecological Aquaculture of Chinese mitten crab (In Chinese), p. 30. 2 Ed. China Agriculture Press, Beijing, China.
48 Wang J, Xu P, Zhou G, Li X, Lu Q, Liu X, et al. 2018. Genetic improvement and breeding practices for Chinese mitten crab, Eriocheir sinensis. J. World Aquac. Soc. 49: 292-301.   DOI
49 Li X, Dong S, Lei Y, Li Y. 2007. The effect of stocking density of Chinese mitten crab Eriocheir sinensis on rice and crab seed yields in rice-crab culture systems. Aquaculture 273: 487-493.   DOI
50 Wang C, Li S, Fu C, Gong X, Huang L, Song X, et al. 2009. Molecular genetic structure and evolution in native and colonized populations of the Chinese mitten crab, Eriocheir sinensis. Biol. Invasions. 11: 389-399.   DOI