Histopathological and transcriptomic analyses of Larimichthys polyactis infected with Vibrio harveyi

doi:10.3969/j.issn.1004-1524.20250031

Acta Agriculturae Zhejiangensis ›› 2025, Vol. 37 ›› Issue (12): 2479-2493.DOI: 10.3969/j.issn.1004-1524.20250031

• Animal Science • Previous Articles Next Articles

Histopathological and transcriptomic analyses of Larimichthys polyactis infected with Vibrio harveyi

HUANG Huiling¹(), HAN Mingming²^,^*(), PAN Xinyu³, ZHAO Xudong¹, XIE Zhigang², XU Jianbin³, LOU Bao²

1. School of Fishery, Zhejiang Ocean University, Zhoushan 316022, Zhejiang, China
2. Institute of Hydrobiology, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China
3. College of Biological and Environmental Sciences, Zhejiang Wanli University, Ningbo 315100, Zhejiang, China

Received:2025-01-13 Online:2025-12-25 Published:2026-01-09

Abstract

Abstract:

To investigate the immune response mechanisms of fish to Vibrio harveyi, this study used small yellow croaker (Larimichthys polyactis) as the material, and transcriptome sequencing and histopathological examination were conducted on the liver, gill filament, and skin after infection with Vibrio harveyi. The results showed that infected fish exhibited scale detachment, skin ulceration, and severe gill congestion. Microscopic examination revealed necrosis of the skin surface, necrosis of gill epithelial cells and structural damage in the gill lamellae, atrophy of liver parenchyma, and vacuolar degeneration of liver cells. Transcriptome analysis indicated the activation of multiple immune-related signaling pathways in the liver, gills, and skin of infected fish, including ECM receptor interaction, JAK-STAT signaling pathway, cytokine cytokine receptor interaction, nucleotide-binding oligomerization domain (NOD)-like receptor signaling pathway, RIG-I like receptor signaling pathway, Toll-like receptor signaling pathway, and cytoplasmic DNA sensing pathway. This study elucidates the molecular mechanisms underlying the multi-tissue pathological damage induced by V. harveyi infection in small yellow croaker at the gene and signaling pathway levels, providing a theoretical basis for future research on disease prevention and control strategies.

Key words: Larimichthys polyactis, Vibrio harveyi, transcriptomics, histopathology, immune pathway

CLC Number:

S941.429

HUANG Huiling, HAN Mingming, PAN Xinyu, ZHAO Xudong, XIE Zhigang, XU Jianbin, LOU Bao. Histopathological and transcriptomic analyses of Larimichthys polyactis infected with Vibrio harveyi[J]. Acta Agriculturae Zhejiangensis, 2025, 37(12): 2479-2493.

Figures/Tables 12

Table 1 Primer sequences for qPCR

基因名称Gene name	正向引物序列Forward primer sequence(5'→3')	反向引物序列Reverse primer sequence(5'→3')
IL-1β	CGCTGAGAACCGCAAAGTTC	TCCCCATCCCTATGGCAAGA
CXCL12	TGGCTGCGTTCATGGTGATA	TGGCAATCACTTGGAAGGGG
CD40	ATCTGCACTTTCAGGCTCCC	GGTTCACAGGTTTTGTGCGG
GHR	TACCTGGCGAGGGGTATCAA	ACTGTGTAGTCTGCAACGGG
β-actin	GACCTGACAGACTACCTCATG	AGTTGAAGGTGGTCTCGTGGA

Fig.1 Clinical symptoms and gill anatomy of infected little yellow croaker

Fig.2 BLAST comparison results of strain

Fig.3 Histopathological changes of skin, gill filament and liver of small yellow croaker infected with Vibrio harveyi A, Skin on the side of the body of healthy small yellow croaker; B, Skin of infected small yellow croaker; e, Outer epidermis; d, Inner dermis; m, Subcutaneous muscular layer; C, Gill filament of healthy small yellow croaker; D, Gill filament of infected small yellow croaker, the gill filament ends and gill vesicles were swollen and hypertrophied (red arrow), and the epithelium of the gill vesicles disintegrated (black arrow); E, Liver from the healthy control group of small yellow croaker; F, Liver of infected small yellow croaker, with varying sizes of vacuoles (red asterisk) in the cytoplasm.

Table 2 Sequencing data statistics

样本 Sample	原始数据 Raw read	清洁数据 Clean read	清洁碱基 Clean base/10⁶	错误率 Error rate	Q20/%	Q30/%	GC含量 GC content/%
CLT1	25 811 984	25 382 197	3.81	0.040	97.56	93.42	47.60
CLT2	22 604 472	22 261 471	3.34	0.040	97.51	93.04	45.23
CLT3	22 846 568	22 321 730	3.35	0.045	96.07	89.46	45.07
CLT4	21 956 789	21 105 640	3.17	0.045	96.23	89.82	45.94
CGT1	22 563 965	21 938 469	3.29	0.045	96.01	89.48	45.89
CGT2	20 877 706	20 481 017	3.07	0.040	97.76	93.44	49.52
CGT3	21 898 399	21 367 459	3.21	0.045	95.82	89.32	46.48
CGT4	22 199 876	21 659 664	3.25	0.045	96.19	89.62	46.88
CST1	20 117 968	19 684 762	2.95	0.045	96.37	90.12	48.65
CST2	21 091 055	20 753 025	3.11	0.045	96.20	89.82	48.54
CST3	20 946 972	20 508 232	3.08	0.045	96.72	90.66	49.66
CST4	22 411 714	21 951 426	3.29	0.045	96.50	90.16	49.14
TLT1	24 475 009	24 120 187	3.62	0.040	98.18	94.52	47.55
TLT2	22 261 232	21 643 146	3.25	0.045	96.71	90.64	46.44
TLT3	22 053 389	21 382 638	3.21	0.045	96.78	90.70	49.92
TLT4	22 326 636	21 874 132	3.28	0.045	96.75	90.70	48.40
TGT1	21 772 087	21 171 477	3.18	0.045	96.44	90.47	48.39
TGT2	21 576 158	20 786 124	3.12	0.045	96.73	90.78	48.41
TGT3	22 763 423	22 085 161	3.31	0.045	96.60	90.43	48.12
TGT4	22 229 333	21 595 373	3.24	0.045	96.50	90.17	47.91
TST1	21 890 142	21 093 258	3.16	0.045	96.53	90.33	49.22
TST2	22 084 348	21 560 450	3.23	0.045	96.85	90.74	49.21
TST3	21 902 085	21 508 753	3.23	0.045	96.51	90.14	48.20
TST4	22 222 789	21 703 208	3.26	0.045	96.59	90.27	49.08

Fig.4 Numbers of differentially expressed genes in the liver, gill filament, and skin of small yellow croaker infected with Vibrio harveyi TLT, Liver of infected group; TGT, Gill filament of infected group; TST, Skin of infected group; CLT, Liver of healthy group; CGT, Gill filament of healthy group; CST, Skin of healthy group.

Fig.5 GO functional enrichment of differentially expressed genes in the liver of small yellow croaker infected with Vibrio harveyi 1, Single-organism metabolic process; 2, Oxidation-reduction process; 3, Carboxylic acid metabolic process; 4, Organic acid metabolic process; 5, Oxoacid metabolic process;6, Metabolic process; 7, Cellular amino acid metabolic process; 8, Small molecule metabolic process; 9, Alpha-amino acid metabolic process; 10, Organonitrogen compound metabolic process; 11, Single-organism carbohydrate catabolic process; 12, tRNA aminoacylation for protein translation; 13, L-serine metabolic process; 14, Carbohydrate catabolic process; 15, Amino acid activation; 16, tRNA aminoacylation; 17, Serine family amino acid metabolic process; 18, Oxidoreductase activity; 19, Catalytic activity; 20, Iron ion binding; 21, Cofactor binding; 22, NAD binding; 23, Hydroxymethyl-, formyl-and related transferase activity; 24, Small molecule binding; 25, Oxidoreductase activity, acting on the CH—OH group of donors, NAD or NADP as acceptor; 26, Oxidoreductase activity, acting on paired donors, with incorporation or reduction of molecular oxygen; 27, Tetrapyrrole binding; 28, Vitamin binding; 29, Glycine hydroxymethyltransferase activity; 30, Coenzyme binding.

Fig.6 GO functional enrichment of differentially expressed genes in the gill filament of small yellow croaker infected with Vibrio harveyi 1, Gas transport; 2, Oxygen transport; 3, Glutamine family amino acid metabolic process; 4, Immune response; 5, Organic acid metabolic process; 6, Oxoacid metabolic process; 7, Immune system process; 8, Carboxylic acid metabolic process; 9, Troponin complex; 10, Striated muscle thin filament; 11, Myofibril; 12, Sarcomere; 13, Myofilament; 14, Contractile fiber; 15, Contractile fiber part; 16, Hemoglobin complex; 17, Collagen; 18, Extracellular matrix part; 19, Actin cytoskeleton; 20, Extracellular matrix; 21, Calcium ion binding; 22, Hydrolase activity, acting on carbon-nitrogen (but not peptide) bonds; 23, Lipid binding; 24, Carboxyltransferase or carbamoyltransferase activity; 25, Extracellular matrix structural constituent; 26, Phospholipid binding; 27, Oxygen binding; 28, Hydrolase activity, acting on acid anhydrides, catalyzing transmembrane movement of substances; 29, Cytokine activity; 30, Pyridoxal phosphate binding.

Fig.7 GO functional enrichment of differentially expressed genes in the skin of small yellow croaker infected with Vibrio harveyi 1, Oxidation-reduction process; 2, Energy coupled proton transport, decreased electrochemical gradient; 3, ATP synthesis coupled electron transport; 4, Purine-containing compound salvage; 5, ATP biosynthetic process; 6, Nucleoside triphosphate biosynthetic process; 7, Purine nucleoside triphosphate biosynthetic process; 8, Ribonucleoside triphosphate biosynthetic process; 9, Purine ribonucleoside triphosphate biosynthetic process; 10, Purine nucleoside biosynthetic process; 11, Purine ribonucleoside biosynthetic process; 12, Troponin complex; 13, Striated muscle thin filament; 14, Myofibril; 15, Sarcomere; 16, Myofilament; 17, Contractile fiber; 18, Contractile fiber part; 19, Mitochondrial inner membrane; 20, Organelle inner membrane; 21, Mitochondrion; 22, Oxidoreductase activity; 23, Cation-transporting ATPase activity; 24, ATPase activity, coupled to transmembrane movement of ions; 25, Primary active transmembrane transporter activity; 26, P-P-bond-hydrolysis-driven transmembrane transporter activity; 27, ATPase activity, coupled to transmembrane movement of substances; 28, Cation transmembrane transporter activity; 29, ATPase activity, coupled to movement of substances; 30, Hydrolase activity, acting on acid anhydrides, catalyzing transmembrane movement of substances.

Fig.8 KEGG pathway enrichment of differentially expressed genes in liver, gill filament and skin of little yellow croaker infected with Vibrio harvevi(Top 15 of enriched pathways) A, Liver ; B, Gill filament ; C, Skin.

Table 3 Changes of key signaling pathways and their p-values in different tissues of healthy group and infected group of little yellow croakers

信号通路 Signaling pathway	p值p value
信号通路 Signaling pathway	TLT vs CLT	TGT vs CGT	TST vs CST
ECM受体相互作用ECM-receptor interaction	0.053 83	1.55×10^-5	1.80×10^-4
类固醇生物合成Steroid biosynthesis	4.68×10^-5	0.204 51	0.709 55
药物代谢-细胞色素P450 Drug metabolism-cytochrome P450	0.001 61	0.760 06	0.093 75
过氧化物酶体Peroxisome	0.006 07	0.638 46	0.540 21
JAK-STAT信号通路JAK-STAT signaling pathway	0.513 82	8.80×10^-4	0.074 86
细胞因子-细胞因子受体相互作用Cytokine-cytokine receptor interaction	0.719 27	2.50×10^-5	0.014 39
黏着斑Focal adhesion	0.749 86	3.10×10^-4	0.125 39
吞噬体Phagosome	0.950 17	0.009 32	0.804 68
肌动蛋白细胞骨架的调节Regulation of actin cytoskeleton	0.987 48	0.042 31	0.944 52
NOD样受体信号通路NOD-like receptor signaling pathway	0.632 37	0.137 23	0.460 77
RIG-I样受体信号通路RIG-I-like receptor signaling pathway	0.788 59	0.405 46	0.955 60
Toll样受体信号通路Toll-like receptor signaling pathway	0.937 22	0.513 55	0.968 32
MAPK信号通路MAPK signaling pathway	0.999 00	0.854 76	0.800 23
内吞作用Endocytosis	0.998 29	0.849 45	0.998 04
钙信号通路Calcium signaling pathway	0.996 86	0.464 02	0.806 56
胞质DNA感知通路Cytosolic DNA-sensing pathway	0.811 59	0.760 06	0.985 52

Fig.9 Validation results for a subset of differentially expressed genes

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Histopathological and transcriptomic analyses of Larimichthys polyactis infected with Vibrio harveyi

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