Gut microbial profiles and its developmental changes of grass carp (Ctenopharyngodon idella)

doi:10.3969/j.issn.1004-1524.20230519

Acta Agriculturae Zhejiangensis ›› 2024, Vol. 36 ›› Issue (4): 780-789.DOI: 10.3969/j.issn.1004-1524.20230519

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Gut microbial profiles and its developmental changes of grass carp (Ctenopharyngodon idella)

ZHANG Hongfang¹^,²(), QIAN Tao³, JIN Ting³, XIE Xiaoling¹, WU Choufei¹, XIAO Yingping², MA Lingyan²^,^*()

1. College of Life Sciences, Huzhou University, Huzhou 313000, Zhejiang, China
2. State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Agro-Product Safety and Nutrition, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China
3. Agriculture and Rural Affairs Bureau of Kaihua County, Kaihua 324300, Zhejiang, China

Received:2023-04-21 Online:2024-04-25 Published:2024-04-29
Contact: MA Lingyan

Abstract

Abstract:

The study was aim to expolar the diversity of the microbial structure in different intestinal segments during the growth and development processes of grass carp. The experiment was conducted in two parts, Part I: Eight grass carp at 24 months were anesthetized with MS-222 for DNA extraction and 16S rRNA sequencing analysis; Part Ⅱ: 25 grass carp with different ages, including 1 month, 7 months, 15 months and 24 months, were purchased from a typical Kaihua clear water fish breeding base in Kaihua County, Quzhou City, Zhejiang Province. To ensure sufficient sample size and minimize individual differences, the contents of the hindgut segments of each five fish were mixed into a single sample. The contents of grass carp at different months were extracted for DNA extraction and 16S rRNA sequencing analysis. The results indicated that: 1) Alpha diversity analysis showed that the diversity and richness of microbial community in hindgut were significantly higher than those in foregut and midgut (P<0.05); Beta diversity analysis showed that the microbial communities in foregut and midgut were similar, but significantly different from those in hindgut (P<0.05). 2) LEfSE analysis showed that Streptococcus and Ralstonia were dominant bacteria in the foregut. Escherichia-Shigella and Aliihoeflea were dominant bacteria in the midgut segment. Leptolyngbya and Cetobacterium are the main dominant genera in the hindgut. 3) The diversity and richness of microbial community in the hindgut of grass carp significantly decreased from 1 month to 24 months of age (P<0.05); Beta diversity analysis showed that there were significant differences in the microbial structure of the hindgut of spring water grass carp at different months (P<0.05). 4) Heatmap shows that Rubellimicrobium and Synechococcus are the main dominant bacteria in the hindgut at the age of 1 month. Aestuariimicrobium and Streptomyces were the dominant genera in the hindgut intestine of the 7-month-old. Kineosporia and Prevotella were dominant genera in the 15-month-old hindgut, while Vibrio and Mesonia were dominant genera in the 24-month-old hindgut. This indicates that there are differences in the composition and structure of microbia communities in different intestinal segments of grass carp, as well as developmental changes in the structure of gut microbiota during different stages of growth.

Key words: grass carp, microbial community structure, developmental change

CLC Number:

S917.1

ZHANG Hongfang, QIAN Tao, JIN Ting, XIE Xiaoling, WU Choufei, XIAO Yingping, MA Lingyan. Gut microbial profiles and its developmental changes of grass carp (Ctenopharyngodon idella)[J]. Acta Agriculturae Zhejiangensis, 2024, 36(4): 780-789.

Figures/Tables 10

Table 1 Alpha diversity analysis of the intestinal microflora in grass carp (n=8)

样本名称 Sample name	操作分类单元数 OTUs	香农指数 Shannon index	辛普森指数 Simpson index	丰度指数 Chao index
前肠Foregut	272± 27 c	3.23±0.26 b	0.17± 0.04	311.13± 41.68 c
中肠Midgut	524± 12 b	3.51±0.16 ab	0.11± 0.02	603.13± 20.90 b
后肠Hindgut	694± 23 a	3.93±0.21 a	0.09± 0.03	917.88± 29.44 a

Fig.1 Principal comporent analysis of microbial community structure in grass carp (n=8)

Fig.2 Analysis of the intestinal microflora structure in grass carp

Fig.3 Phylogenetic tree of intestinal microflora structure in grass carp

Fig.4 Heatmap of microbial community structure in grass carp (Top 35 genus)

Table 2 Alpha diversity analysis of hindgut microbial of grass carp at different months (n=5)

样本名称 Sample name	操作分类单元数 OTUs	香农指数 Shannon index	辛普森指数 Simpson index	丰度指数 Chao index
1月龄1-month-old	562±106 a	3.74±0.61 a	0.11±0.09 ab	776.00±131.87 a
7月龄7-month-old	475±50 ab	3.60±0.17 a	0.11±0.02 ab	611.20±54.03 b
15月龄15-month-old	470±57 abc	3.54±0.29 a	0.12±0.04 ab	551.00±71.25 bc
24月龄24-month-old	270±85 c	2.30±0.16 b	0.27±0.04 a	292.60±43.90 cd

Fig.5 Principal component analysis of hindgut microbial community structure of grass carp at different months

Fig.6 Hindgut microbial community structure of grass carp at different months

Fig.7 Heatmap of hindgut microbial community structure of grass carp at different months (Top 35 genus)

Fig.8 Microbial composition in water environment at different months

References 25

[1]	EGERTON S, CULLOTY S, WHOOLEY J, et al. The gut microbiota of marine fish[J]. Frontiers in Microbiology, 2018, 9: 873.
[2]	HUANG Q, SHAM R C, DENG Y, et al. Diversity of gut microbiomes in marine fishes is shaped by host-related factors[J]. Molecular Ecology, 2020, 29(24): 5019-5034.
[3]	ROMBOUT J H W M, ABELLI L, PICCHIETTI S, et al. Teleost intestinal immunology[J]. Fish & Shellfish Immunology, 2011, 31(5): 616-626.
[4]	CHEN L M, GARMAEVA S, ZHERNAKOVA A, et al. A system biology perspective on environment-host-microbe interactions[J]. Human Molecular Genetics, 2018, 27(R2): R187-R194.
[5]	MA J Y, PIAO X S, MAHFUZ S, et al. The interaction among gut microbes, the intestinal barrier and short chain fatty acids[J]. Animal Nutrition, 2022, 9: 159-174.
[6]	RAY A K, GHOSH K, RINGØ E. Enzyme-producing bacteria isolated from fish gut: a review[J]. Aquaculture Nutrition, 2012, 18(5): 465-492.
[7]	PARATA L, NIELSEN S, XING X, et al. Age, gut location and diet impact the gut microbiome of a tropical herbivorous surgeonfish[J]. FEMS Microbiology Ecology, 2020, 96(1): fiz179.
[8]	BUTT R L, VOLKOFF H. Gut microbiota and energy homeostasis in fish[J]. Frontiers in Endocrinology, 2019, 10: 9.
[9]	陈小雷, 崔凯, 周蓓蓓, 等. 山泉流水与池塘养殖草鱼营养成分比较[J]. 水产科学, 2020, 39(1): 63-71.
	CHEN X L, CUI K, ZHOU B B, et al. Comparison of nutrient composition in grass carp Ctenopharyngodon idellus cultured in spring flowing water and in a routine pond[J]. Fisheries Science, 2020, 39(1): 63-71. (in Chinese with English abstract)
[10]	FENG W W, ZHANG J, JAKOVLIĆ I, et al. Gut segments outweigh the diet in shaping the intestinal microbiota composition in grass carp Ctenopharyngodon idellus[J]. AMB Express, 2019, 9(1): 44.
[11]	MOWAT A M, AGACE W W. Regional specialization within the intestinal immune system[J]. Nature Reviews Immunology, 2014, 14(10): 667-685.
[12]	STEPHENS W Z, BURNS A R, STAGAMAN K, et al. The composition of the zebrafish intestinal microbial community varies across development[J]. The ISME Journal, 2016, 10(3): 644-654.
[13]	YOSHIDA M A, TANABE T, AKIYOSHI H, et al. Gut microbiota analysis of Blenniidae fishes including an algae-eating fish and clear boundary formation among isolated Vibrio strains[J]. Scientific Reports, 2022, 12: 4642.
[14]	YANG G, JIAN S Q, CAO H Z, et al. Changes in microbiota along the intestine of grass carp (Ctenopharyngodon idella): community, interspecific interactions, and functions[J]. Aquaculture, 2019, 498: 151-161.
[15]	丁红秀, 李忠莹, 刘俊, 等. 不同生境草鱼肠道微生物组成和群落特征分析[J]. 微生物学报, 2021, 61(3): 729-739.
	DING H X, LI Z Y, LIU J, et al. Comparison of intestinal microbiome composition and community characteristics of grass carp from different habitats[J]. Acta Microbiologica Sinica, 2021, 61(3): 729-739. (in Chinese with English abstract)
[16]	MORAN D, TURNER S J, CLEMENTS K D. Ontogenetic development of the gastrointestinal microbiota in the marine herbivorous fish Kyphosus sydneyanus[J]. Microbial Ecology, 2005, 49(4): 590-597.
[17]	NAVARRETE P, ESPEJO R T, ROMERO J. Molecular analysis of microbiota along the digestive tract of juvenile Atlantic salmon (Salmo salar L.)[J]. Microbial Ecology, 2009, 57(3): 550-561.
[18]	WEI J, GUO X W, LIU H, et al. The variation profile of intestinal microbiota in blunt snout bream (Megalobrama amblycephala) during feeding habit transition[J]. BMC Microbiology, 2018, 18(1): 99.
[19]	WANG S T, MENG X Z, ZHANG J H, et al. 16S rRNA sequencing analysis of the correlation between the intestinal microbiota and body-mass of grass carp (Ctenopharyngodon idella)[J]. Comparative Biochemistry and Physiology Part D, Genomics & Proteomics, 2020, 35: 100699.
[20]	LU Y T, ZHANG P J, LI W, et al. Comparison of gut microbial communities, free amino acids or fatty acids contents in the muscle of wild Aristichthys nobilis from Xinlicheng Reservoir and Chagan Lake[J]. BMC Microbiology, 2022, 22(1): 32.
[21]	WU S G, WANG G T, ANGERT E R, et al. Composition, diversity, and origin of the bacterial community in grass carp intestine[J]. PLoS One, 2012, 7(2): e30440.
[22]	GAO Y M, ZOU K S, ZHOU L, et al. Deep insights into gut microbiota in four carnivorous coral reef fishes from the South China Sea[J]. Microorganisms, 2020, 8(3): 426.
[23]	HAO Y T, WU S G, XIONG F, et al. Succession and fermentation products of grass carp (Ctenopharyngodon idellus) hindgut microbiota in response to an extreme dietary shift[J]. Frontiers in Microbiology, 2017, 8: 1585.
[24]	LIU H, GUO X W, GOONERATNE R, et al. The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels[J]. Scientific Reports, 2016, 6: 24340.
[25]	LIU Y Q, LI X H, LI Y F, et al. Gut microbiomes of cyprinid fish exhibit host-species symbiosis along gut trait and diet[J]. Frontiers in Microbiology, 2022, 13: 936601.

Gut microbial profiles and its developmental changes of grass carp (Ctenopharyngodon idella)

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