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Article(id=1192149546315694160, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1192149543010582589, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20250224, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1742400000000, receivedDateStr=2025-03-20, revisedDate=null, revisedDateStr=null, acceptedDate=1745337600000, acceptedDateStr=2025-04-23, onlineDate=1762160200909, onlineDateStr=2025-11-03, pubDate=1756915200000, pubDateStr=2025-09-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1762160200909, onlineIssueDateStr=2025-11-03, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1762160200909, creator=13701087609, updateTime=1762160200909, updator=13701087609, issue=Issue{id=1192149543010582589, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='10', pageStart='4241', pageEnd='4713', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1762160200113, creator=13701087609, updateTime=1762160638682, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1192151382586175735, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1192149543010582589, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1192151382586175736, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1192149543010582589, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=4593, endPage=4606, ext={EN=ArticleExt(id=1192149547519459410, articleId=1192149546315694160, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Disruptive effects of fluoride exposure on the insect gut microecosystem, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

[Objective] To investigate the effects of fluoride exposure on the gut microecosystem of the model insect Bombyx mori and elucidate the toxic mechanisms of fluoride under different conditions on insect hosts. [Methods] We measured physiological enzyme activity changes in the gut tissue of B. mori following fluoride exposure and observed histopathological changes by using hematoxylin and eosin (HE) staining. We also analyzed the dynamic changes in gut microbiota by using 16S rRNA amplicon sequencing and examined the expression changes of immune-related genes in gut tissue by qPCR. [Results] Fluoride exposure significantly increased the malondialdehyde (MDA) level and decreased the reduced glutathione (GSH) level in the gut tissue. Enzyme activities of catalase (CAT), superoxide dismutase (SOD), acetylcholinesterase (AChE), carboxylesterase (CarE), alkaline phosphatase (AKP/ALP), and lactate dehydrogenase (LDH) were also markedly suppressed. Additionally, we observed epithelial cell rupture and separation from the basement membrane. The Toll immune pathway was inhibited, which resulted in significantly reduced expression of antimicrobial peptide genes, such as attacin, cecropin, lebocin, and lysozyme. Gut microbiota analysis revealed significant declines in the relative abundances of Glutamicibacter, Staphylococcus, Acinetobacter, and Methylobacterium. The gut microbiota exhibited notable structural heterogeneity with strengthened functions related to metabolic pathways and biosynthesis of secondary metabolites. [Conclusion] Fluoride exposure significantly weakened the host insect’s antioxidant capacity, basal metabolism, and immune function, damaged the integrity of gut tissue, and caused gut microbiota dysbiosis. This disruption of the gut microecosystem might be a major factor contributing to reduced insect species diversity and biomass.

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【目的】 探讨氟暴露对模式昆虫家蚕肠道微生态系统的影响，深入解析氟在不同条件下对昆虫宿主的毒害机制。 【方法】 通过测定氟暴露后家蚕肠道组织中多种生理相关酶活性的变化，结合苏木精-伊红(hematoxylin-eosin, HE)染色观察肠道组织的病理学变化。同时，采用16S rRNA基因扩增子测序技术分析肠道菌群的动态变化，并利用实时定量聚合酶链式反应技术检测肠道组织中免疫相关基因的表达变化。 【结果】 氟暴露显著增加了家蚕肠道组织中丙二醛(malondialdehyde, MDA)的含量，降低了还原型谷胱甘肽(glutathione, GSH)水平，并削弱了过氧化氢酶(catalase, CAT)、超氧化物歧化酶(superoxide dismutase, SOD)、乙酰胆碱酯酶(acetylcholinesterase, AChE)、羧酸酯酶(carboxylesterase, CarE)、碱性磷酸酶(alkaline phosphatase, AKP/ALP)和乳酸脱氢酶(lactate dehydrogenase, LDH)等的活性；此外，肠道上皮细胞碎裂，细胞与基底膜分离。Toll免疫调节途径受到抑制，导致抗菌肽蛋白基因(如attacin、cecropin、lebocin和lysozyme)的表达显著下降。肠道菌群分析显示，谷氨酸杆菌(Glutamicibacter)、葡萄球菌(Staphylococcus)、不动杆菌(Acinetobacter)和甲基杆菌(Methylobacterium)的相对丰度显著减少，且菌群结构发生显著异质性变化。菌群功能预测显示，其代谢途径(metabolic pathways)和次级代谢物生物合成(biosynthesis of secondary metabolites)功能明显增强。 【结论】 氟暴露显著削弱昆虫宿主的抗氧化能力、基础代谢和免疫功能，损害肠道组织的结构完整性，并导致肠道菌群失衡。这种对肠道微生态系统稳态的破坏可能是引发昆虫物种多样性降低和生物量减少的重要原因。

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作者贡献声明

李冠楠：提出概念，数据收集与管理，数据分析，获取基金，执行调研，完成呈现，方法论，撰写文章并审阅；肖祎：提出概念，数据收集与管理，执行调研，验证，完成呈现，文章编辑；卢思君：执行调研，验证，文章编辑；李承翰：执行调研，验证；温逍治：执行调研，验证；赵天福：项目管理，提供资源，监督管理。

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A: Malondialdehyde; B: Reduced glutathione; C: Catalase; D: Superoxide dismutase; E: Acetylcholinesterase; F: Carboxylesterase; G: Alkaline phosphatase; H: Lactate dehydrogenase., figureFileSmall=LQRf7LG94ECAeCHgyoGwrA==, figureFileBig=F3HueZ41xJ3AkyGDOEmoPw==, tableContent=null), ArticleFig(id=1192161024812921184, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=CN, label=图1, caption=氟暴露对昆虫宿主生理代谢酶系的影响。A：丙二醛；B：还原型谷胱甘肽；C：过氧化氢酶；D：超氧化物歧化酶；E：乙酰胆碱酯酶；F：羧酸酯酶；G：碱性磷酸酶；H：乳酸脱氢酶。, figureFileSmall=LQRf7LG94ECAeCHgyoGwrA==, figureFileBig=F3HueZ41xJ3AkyGDOEmoPw==, tableContent=null), ArticleFig(id=1192161024909390177, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=EN, label=Figure 2, caption=Histological observation of the insect gut after fluoride exposure., figureFileSmall=wrkkoGUVUrbhguJvmWsYlA==, figureFileBig=xh2TYjbk+H4aBVUV0hKZKg==, tableContent=null), ArticleFig(id=1192161024976499042, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=CN, label=图2, caption=氟暴露后昆虫肠道的组织形态观察, figureFileSmall=wrkkoGUVUrbhguJvmWsYlA==, figureFileBig=xh2TYjbk+H4aBVUV0hKZKg==, tableContent=null), ArticleFig(id=1192161025039413603, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=EN, label=Figure 3, caption=Effects of fluoride on the gut barrier and expression of related immune genes in insects. A: Cautus; B: Spz; C: Rel; D: Att2; E: CecA; F: CecB6; G: CecD; H: Leb1; I: Lys., figureFileSmall=UbkL3xjk0W0MpFfiX7kdvQ==, figureFileBig=YU8qTp+Toog3EMN/vNFvOg==, tableContent=null), ArticleFig(id=1192161025093939556, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=CN, label=图3, caption=氟暴露对昆虫肠道屏障和相关免疫基因表达的影响, figureFileSmall=UbkL3xjk0W0MpFfiX7kdvQ==, figureFileBig=YU8qTp+Toog3EMN/vNFvOg==, tableContent=null), ArticleFig(id=1192161025152659813, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=EN, label=Figure 4, caption=Effects of fluoride on the structure of gut microbiota structure in insect hosts. A: The phylum and genus levels of intestinal microbiota; B: Alpha diversity estimated by the number of observed species and the Shannon, Chao1, and Sobs indexes; C: PCoA based on the weighted UniFrac distance matrix from all the samples; D: Analysis of the microbial dysbiosis index; E: Difference analysis of the predominant bacterial genera; F: LEfSe comparison of the most differentially abundant taxa among the groups., figureFileSmall=B/c+WOAPblbQ6uvmV84P6Q==, figureFileBig=t4NUQyIYKh021e12gkAw0A==, tableContent=null), ArticleFig(id=1192161025202991462, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=CN, label=图4, caption=氟暴露对昆虫宿主肠道菌群结构的影响。A：细菌分类的门水平和属水平；B：菌群多样性指数分析；C：菌群组成PCoA分析；D：菌群失衡指数分析；E：菌群组成差异分析；F：菌群组成丰度的LEfSe分析。, figureFileSmall=B/c+WOAPblbQ6uvmV84P6Q==, figureFileBig=t4NUQyIYKh021e12gkAw0A==, tableContent=null), ArticleFig(id=1192161025286877543, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=EN, label=Figure 5, caption=Effects of fluoride on the function of gut microbiota in insect hosts. A: Classifications of the intestinal microbiota based on COG categories; B: Examination of changes in KEGG pathways within insectintestinal microbiota after fluoride exposure; C: Analysis of the phenotypic traits exhibited by silkworm intestinal microbiota., figureFileSmall=Efzep3VpQVugZqtfyfcYjw==, figureFileBig=tqpi5ILMynI1o5adf8PB3A==, tableContent=null), ArticleFig(id=1192161025370763624, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=CN, label=图5, caption=氟暴露对昆虫宿主肠道菌群功能的影响。A：肠道菌群的COG分类；B：肠道菌群的KEGG代谢通路分析；C：肠道菌群的组成表型特征。, figureFileSmall=Efzep3VpQVugZqtfyfcYjw==, figureFileBig=tqpi5ILMynI1o5adf8PB3A==, tableContent=null), ArticleFig(id=1192161025421095273, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=EN, label=Table 1, caption=

Primers used in the RT-qPCR of the related genes in the silkworm

, figureFileSmall=null, figureFileBig=null, tableContent=
Gene namePrimer sequences (5′→3′)Amplicon size (bp)
Actin3F: GCACGTGTAGCTGCGAAAAA147
R: TTAAACAATGGCGGCTGTGC
Att2F: TTCAAACAGAAGGTGGGC210
R: GACGGAGATTGGAACAGG
CecAF: CCAAAGACGCATTTAGCTTG136
R: ACTCGGTCACTCTGAGAAAG
CeB6F: TCCTTCGTCTTCGCTCTG164
R: GATGCCGTCACGGATGTT
CecDF: CTCCCGGCAACTTCTTCA186
R: CGAACCCTCTGACCCATT
Leb1F: GGTTCATCCAGCCGACCTAC292
R: GTGTTACGGTGGCTCTCGAT
LysF: CAGCCGTGACACATCCAAGA140
R: TCAGGAGGTCGGAGCACTTA
CactusF: CCTCCGCTGTATCTACTGTTCC188
R: ATGGCATTACCACTCATCACC
SpzF: AGCGTAAGTCAGTCG CCAAA346
R: GAGAGTCGTCCGTTTGAGCA
RelF: GAACAGCCACAGGACTACTTTA293
R: ATGATACCCATTCCACCGAAC
), ArticleFig(id=1192161025475621226, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1192149546315694160, language=CN, label=表1, caption=

荧光定量分析所用引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
Gene namePrimer sequences (5′→3′)Amplicon size (bp)
Actin3F: GCACGTGTAGCTGCGAAAAA147
R: TTAAACAATGGCGGCTGTGC
Att2F: TTCAAACAGAAGGTGGGC210
R: GACGGAGATTGGAACAGG
CecAF: CCAAAGACGCATTTAGCTTG136
R: ACTCGGTCACTCTGAGAAAG
CeB6F: TCCTTCGTCTTCGCTCTG164
R: GATGCCGTCACGGATGTT
CecDF: CTCCCGGCAACTTCTTCA186
R: CGAACCCTCTGACCCATT
Leb1F: GGTTCATCCAGCCGACCTAC292
R: GTGTTACGGTGGCTCTCGAT
LysF: CAGCCGTGACACATCCAAGA140
R: TCAGGAGGTCGGAGCACTTA
CactusF: CCTCCGCTGTATCTACTGTTCC188
R: ATGGCATTACCACTCATCACC
SpzF: AGCGTAAGTCAGTCG CCAAA346
R: GAGAGTCGTCCGTTTGAGCA
RelF: GAACAGCCACAGGACTACTTTA293
R: ATGATACCCATTCCACCGAAC
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氟暴露对昆虫肠道微生态系统的损害影响
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李冠楠 1 , 肖祎 1 , 卢思君 2 , 李承翰 2 , 温逍治 2 , 赵天福 1
微生物学报 | 研究报告 2025,65(10): 4593-4606
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微生物学报 | 研究报告 2025, 65(10): 4593-4606
氟暴露对昆虫肠道微生态系统的损害影响
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李冠楠1, 肖祎1, 卢思君2, 李承翰2, 温逍治2, 赵天福1
作者信息
  • 1西南大学 蚕桑纺织与生物质科学学院，资源昆虫高效养殖与利用全国重点实验室，重庆
  • 2西南大学 西塔学院，重庆
Disruptive effects of fluoride exposure on the insect gut microecosystem
Guannan LI1, Yi XIAO1, Sijun LU2, Chenghan LI2, Xiaozhi WEN2, Tianfu ZHAO1
Affiliations
  • 1State Key Laboratory of Resource Insects, College of Sericulture, Textile and Biomass Sciences, Southwest University, Chongqing, China
  • 2Westa College, Southwest University, Chongqing, China
出版时间: 2025-09-04 doi: 10.13343/j.cnki.wsxb.20250224
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【目的】 探讨氟暴露对模式昆虫家蚕肠道微生态系统的影响，深入解析氟在不同条件下对昆虫宿主的毒害机制。 【方法】 通过测定氟暴露后家蚕肠道组织中多种生理相关酶活性的变化，结合苏木精-伊红(hematoxylin-eosin, HE)染色观察肠道组织的病理学变化。同时，采用16S rRNA基因扩增子测序技术分析肠道菌群的动态变化，并利用实时定量聚合酶链式反应技术检测肠道组织中免疫相关基因的表达变化。 【结果】 氟暴露显著增加了家蚕肠道组织中丙二醛(malondialdehyde, MDA)的含量，降低了还原型谷胱甘肽(glutathione, GSH)水平，并削弱了过氧化氢酶(catalase, CAT)、超氧化物歧化酶(superoxide dismutase, SOD)、乙酰胆碱酯酶(acetylcholinesterase, AChE)、羧酸酯酶(carboxylesterase, CarE)、碱性磷酸酶(alkaline phosphatase, AKP/ALP)和乳酸脱氢酶(lactate dehydrogenase, LDH)等的活性；此外，肠道上皮细胞碎裂，细胞与基底膜分离。Toll免疫调节途径受到抑制，导致抗菌肽蛋白基因(如attacin、cecropin、lebocin和lysozyme)的表达显著下降。肠道菌群分析显示，谷氨酸杆菌(Glutamicibacter)、葡萄球菌(Staphylococcus)、不动杆菌(Acinetobacter)和甲基杆菌(Methylobacterium)的相对丰度显著减少，且菌群结构发生显著异质性变化。菌群功能预测显示，其代谢途径(metabolic pathways)和次级代谢物生物合成(biosynthesis of secondary metabolites)功能明显增强。 【结论】 氟暴露显著削弱昆虫宿主的抗氧化能力、基础代谢和免疫功能，损害肠道组织的结构完整性，并导致肠道菌群失衡。这种对肠道微生态系统稳态的破坏可能是引发昆虫物种多样性降低和生物量减少的重要原因。

模式昆虫家蚕  /  氟暴露  /  免疫  /  生理指标  /  肠道菌群

[Objective] To investigate the effects of fluoride exposure on the gut microecosystem of the model insect Bombyx mori and elucidate the toxic mechanisms of fluoride under different conditions on insect hosts. [Methods] We measured physiological enzyme activity changes in the gut tissue of B. mori following fluoride exposure and observed histopathological changes by using hematoxylin and eosin (HE) staining. We also analyzed the dynamic changes in gut microbiota by using 16S rRNA amplicon sequencing and examined the expression changes of immune-related genes in gut tissue by qPCR. [Results] Fluoride exposure significantly increased the malondialdehyde (MDA) level and decreased the reduced glutathione (GSH) level in the gut tissue. Enzyme activities of catalase (CAT), superoxide dismutase (SOD), acetylcholinesterase (AChE), carboxylesterase (CarE), alkaline phosphatase (AKP/ALP), and lactate dehydrogenase (LDH) were also markedly suppressed. Additionally, we observed epithelial cell rupture and separation from the basement membrane. The Toll immune pathway was inhibited, which resulted in significantly reduced expression of antimicrobial peptide genes, such as attacin, cecropin, lebocin, and lysozyme. Gut microbiota analysis revealed significant declines in the relative abundances of Glutamicibacter, Staphylococcus, Acinetobacter, and Methylobacterium. The gut microbiota exhibited notable structural heterogeneity with strengthened functions related to metabolic pathways and biosynthesis of secondary metabolites. [Conclusion] Fluoride exposure significantly weakened the host insect’s antioxidant capacity, basal metabolism, and immune function, damaged the integrity of gut tissue, and caused gut microbiota dysbiosis. This disruption of the gut microecosystem might be a major factor contributing to reduced insect species diversity and biomass.

model insect Bombyx mori  /  fluoride exposure  /  immunity  /  physiological indexes  /  gut microbiota
李冠楠, 肖祎, 卢思君, 李承翰, 温逍治, 赵天福. 氟暴露对昆虫肠道微生态系统的损害影响. 微生物学报, 2025 , 65 (10) : 4593 -4606 . DOI: 10.13343/j.cnki.wsxb.20250224
Guannan LI, Yi XIAO, Sijun LU, Chenghan LI, Xiaozhi WEN, Tianfu ZHAO. Disruptive effects of fluoride exposure on the insect gut microecosystem[J]. Acta Microbiologica Sinica, 2025 , 65 (10) : 4593 -4606 . DOI: 10.13343/j.cnki.wsxb.20250224
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随着人类文明的不断发展，地球上大部分可耕种土地已被用于农业和城市建设，大面积森林的破坏导致环境中二氧化碳(CO₂)浓度持续升高，从而引发一系列全球性极端气候事件[1]。与此同时，大规模的社会和工业活动带来了严重的环境污染问题，其中氟化物是主要的污染物之一[2]。调查显示，山西、内蒙古、陕西、甘肃、宁夏、青海、新疆、四川和贵州等省(自治区)是我国氟污染严重的地区[3]。昆虫作为维持自然界生物链稳定性的基础环节，不仅是高等动物的重要食物来源，也是植物授粉的重要媒介[4]。目前已知地球上的昆虫种类多达近百万种。近年来研究报告显示，昆虫的物种多样性、丰富度和生物量正在急剧下降，而生态环境的变化及污染物的持续增加被认为是主要原因[5]。研究表明，生物体过量接触氟化物会导致体内氟负荷增加，从而引发多种健康问题，包括氟骨症、炎症性肠病和神经系统紊乱等[6-7]。此外，氟暴露会显著改变昆虫宿主的肠道菌群结构，如肠球菌属(Enterococcus)细菌减少，而葡萄球菌属(Staphylococcus)细菌显著增加[8]，并且分泌多种消化酶的细菌种群丰度也有所降低[9]，进一步削弱了宿主的生理功能。Li等[10]研究表明，氟暴露还可通过破坏菌-肠-血屏障导致昆虫宿主死亡。然而，目前对于长短期氟暴露对昆虫微生态系统毒害机制的研究仍不够深入，尚需进一步探索。
昆虫肠道内居住着广泛多样的微生物，它们是昆虫微生态系统中的核心组分。微生态系统由肠道菌群、肠上皮组织和肠道免疫构成，在维持宿主机体稳态中扮演着至关重要的角色[11]。研究表明肠道菌群能够抵御外源致病微生物并维持肠道微生态系统的平衡；此外，昆虫肠道菌群能参与消化吸收，并协助宿主免疫系统以抵御感染[12-13]。家蚕(Bombyxmori L.)不仅是特种经济饲养昆虫，还作为种间模式生物广泛应用于微生物与宿主互作、药物筛选、生理学、医学和毒理学等科研领域[14]。有研究指出，家蚕肠道内的微生物菌群能够产生多种酶，如蛋白酶、淀粉酶、脂肪酶、纤维素酶、脲酶、明胶酶和木聚糖酶等，这些酶在家蚕肠道内对消化和免疫起着重要作用[15-16]。肠道菌群可能受食物营养成分、饮食环境和其他微生物的改变而发生变化[17-19]，其中食物环境的改变是导致昆虫生理活力和肠道菌群改变的最重要因素之一。Zeng等[20]研究表明，家蚕的抗氟性与其蚕沙代谢物中的氟浓度相关，抗氟性较强的家蚕品种其蚕沙中氟含量较高。此外，氟暴露后，抗氟家蚕的肠道核心菌群仅相对丰度下降，而氟敏家蚕的肠道核心菌群物种组成则发生显著改变[21]。
目前，虽有研究表明氟暴露会影响昆虫肠道菌群的组成，但关于不同条件氟暴露对昆虫微生态系统的影响，特别是肠道上皮形态和肠道免疫响应的研究尚未见报道。本研究以家蚕为模式昆虫，通过生理酶活性测定和石蜡切片技术观察氟暴露对肠道组织形态和功能的影响，结合16S rRNA基因测序分析肠道菌群在不同氟暴露条件下的动态变化，并利用逆转录实时定量聚合酶链式反应探究氟暴露对宿主免疫响应的影响。多种生物学技术的综合应用，有助于更真实地揭示长短期氟暴露对昆虫宿主的损害，为理解氟暴露导致昆虫种群多样性和数量下降提供理论参考。
1 材料与方法
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1.1 材料
1.1.1 供试家蚕
实验所用家蚕品种为生产用种‘菁松×皓月’由重庆市蚕业科学技术研究院提供。
1.1.2 主要试剂和仪器
FastKing RT反转录试剂盒，天根生化科技(北京)有限公司；TB GreenTM Premix Ex TaqTM荧光定量试剂盒、TRIzol试剂，TaKaRa公司；E.Z.N.A.® Soil DNA Kit，Omega公司；特异性引物合成及酶活性试剂盒，生工生物工程(上海)有限公司。
切片机，徕卡仪器有限公司；组织包埋机和烘片机，深圳市科迪生物科技有限公司；光学显微镜及成像系统，尼康株式会社；多功能酶标仪，Agilent公司；Qubit 4.0、NanoDrop 2000超微量分光光度计，ThermoFisher Scientific公司；实时荧光定量PCR系统，ABI公司；高通量测序Illumina MiSeq平台，Illumina公司。
1.2 家蚕饲养和样本提取
蚕种按照常规方法催青并饲养至4龄初龄。本研究将家蚕分为对照组(CK组)、低浓度处理组(CH组)和高浓度处理组(AC组)。对照组家蚕饲喂经清水浸泡10 min后自然晾干的新鲜桑叶；CH组和AC组分别饲喂以50 mg/kg和200 mg/kg 氟化钠(sodium fluoride, NaF)溶液浸泡10 min后自然晾干的新鲜桑叶[20,22]。CH组家蚕自4龄初龄开始添加处理，AC组家蚕自5龄初龄开始添加处理。所有组的家蚕均饲养至5龄第3天后断食，并饥饿处理24 h以备解剖。每个处理组随机取5个样本，每个样本至少包含3只家蚕个体。
取饥饿处理后的家蚕，用75%的乙醇对体表进行消毒，并在酒精灯火焰下轻轻灼烧。随后，在无菌条件下解剖家蚕，获取其肠道组织及内容物，分别收集于已灭菌的1.5 mL离心管中。部分肠道组织置于4%的多聚甲醛溶液中固定24 h后转移至75%的乙醇溶液中，用于切片实验；另一部分肠道组织经RNA提取和反转录为cDNA后用于荧光定量分析。
1.3 抗氧化酶系和基础代谢酶系测定
本研究所涉及的生理标志物包括丙二醛(malondialdehyde, MDA)、还原型谷胱甘肽(reduced glutathione, GSH)、过氧化氢酶(catalase, CAT)、超氧化物歧化酶(superoxide dismutase, SOD)、乙酰胆碱酯酶(acetylcholinesterase, AChE)、羧酸酯酶(carboxylesterase, CarE)、碱性磷酸酶(alkaline phosphatase, AKP/ALP)和乳酸脱氢酶(lactate dehydrogenase, LDH)等。解剖获得的家蚕肠道组织在冰浴条件下制备组织匀浆，经5 000 r/min离心15 min后，取上清液并置于4 ℃冰箱保存备用。所有生理标志物的检测均按照生工生物工程(上海)股份有限公司提供的操作说明进行，每项指标均进行3次生物学重复。
1.4 肠道组织的形态学观察
解剖获得的家蚕肠道组织先在4%多聚甲醛中固定24 h，随后经过乙醇溶液逐级脱水、二甲苯透明处理及石蜡包埋，制成连续切片，切片厚度为5 µm。切片在45-55 ℃烘干后，进行二甲苯脱蜡处理。之后，用苏木精-伊红(hematoxylin-eosin, HE)染色，最后用中性树胶封片。染色后的切片通过成像系统(尼康株式会社)进行观察和拍照。
1.5 肠道组织的免疫响应分析
使用TRIzol试剂提取家蚕肠道组织的总RNA，随后通过NanoDrop 2000超微量分光光度计测定RNA的浓度和纯度。通过1%琼脂糖凝胶电泳检测RNA的完整性后，使用FastKing RT反转录试剂盒合成cDNA，并将其置于-20 ℃保存备用。
采用逆转录实时定量聚合酶链式反应(quantitative real-time PCR, RT-qPCR)法检测肠道组织中相关免疫基因的表达变化。以Actin3作为内参基因，所有引物序列见表1。RT-qPCR反应体系(20 μL)：2×NovoStart® Fast SYBR qPCR SuperMix 10 μL，上、下游引物(10 μmol/L)各 1 μL，DNA模板1 μL，ddH2O补足至20 μL。反应条件：95 ℃预变性3 min；95 ℃变性30 s，55 ℃退火45 s，72 ℃延伸30 s，共38个循环。每个处理组的样品均进行3个生物学重复。免疫基因表达的倍数变化用2-ΔΔCt法计算[23]。
1.6 肠道菌群的动态变化分析
使用E.Z.N.A.® Soil DNA Kit从家蚕肠道内容物中提取细菌基因组DNA，并通过1%的琼脂糖凝胶电泳检测基因组DNA的质量，随后利用NanoDrop 2000超微量分光光度计测定DNA的浓度和纯度。以提取的DNA为模板，使用带有barcode序列的上游引物338F和下游引物806R对16S rRNA基因的V3-V4可变区进行PCR扩增。PCR反应体系：5×TransStart FastPfu缓冲液4 μL，dNTPs (2.5 mmol/L) 2 μL，上、下游引物(5 µmol/L)各0.8 μL，TransStart FastPfu DNA聚合酶(2.5 U/μL) 0.4 μL，模板DNA 10 ng，ddH₂O补足至20 μL。PCR扩增程序：95 ℃预变性3 min；95 ℃变性30 s，55 ℃退火30 s，72 ℃延伸30 s，共27个循环；72 ℃终延伸10 min；4 ℃保存。PCR产物通过2%琼脂糖凝胶回收，并用Qubit 4.0进行定量检测。使用NEXTflex Rapid DNA-Seq Kit对纯化后的PCR产物进行建库，最后利用Illumina NextSeq 2000平台进行扩增子测序。
对原始高通量测序数据使用fastp和FLASH软件[24]进行质控和序列拼接，利用QIIME 2软件[25]进行降噪处理，得到扩增子序列变体(amplicon sequence variants, ASVs)。基于Silva 16S rRNA基因数据库[26]，使用QIIME 2软件对ASVs进行物种分类学分析，并使用PICRUSt2 (v.2.2.0)软件进行功能预测分析。
1.7 统计分析
所有实验数据均进行至少3次生物学重复，结果以平均值±标准差表示。利用GraphPad Prism 10软件进行数据分析和作图，统计分析采用Student’s t检验和Kruskal-Wallis H检验。P<0.05表示数据之间存在显著性差异。
2 结果与分析
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2.1 氟暴露对家蚕生理代谢的影响
本研究通过测定MDA、GSH、SOD和CAT等生物标志物的含量和酶活性，探讨氟暴露对家蚕肠道组织的氧化损伤情况。如图1所示，CH组与CK组家蚕肠道组织中的MDA含量无显著差异，而AC组的MDA含量显著高于CK组和CH组。在不同浓度氟暴露下，家蚕肠道组织中的GSH含量均显著下降，与对照组CK组(GSH含量215.50 µg/g)相比，CH组和AC组的GSH含量分别降至117.34 µg/g和88.66 µg/g。此外，氟暴露后家蚕肠道组织中的CAT和SOD酶活性呈现不同变化趋势，但AC组这2种酶的活性均显著低于CK组。与CK组相比，AC组的SOD活性降至CK组的82.52%，而CAT酶活性降至CK组的19.47%。在基础代谢酶系方面，CH组中AChE和CarE的酶活性与CK组无显著差异，而在AC组中这2种酶的活性显著下降，分别为CK组的63.39%和60.24%。同时，氟暴露导致CH和AC组肠道组织中AKP/ALP酶活性显著下降，分别为对照组CK组的71.9%和23.2%。相较于CK组，CH组中的LDH酶活性显著增加至128.8%，而AC组的LDH酶活性则显著下降至CK组的67.8%。这些结果表明氟暴露会引发昆虫体内严重的氧化应激反应和生理代谢失调，且高浓度短期氟暴露对昆虫宿主的抗氧化和基础代谢功能产生更大的影响。
2.2 氟暴露对昆虫中肠组织形态的影响
苏木精-伊红染色法可以将细胞核染成蓝紫色，而将细胞质染成粉红色。根据生理指标检测结果，对家蚕肠道组织进行了组织病理学分析。如图2所示，对照组(CK)家蚕肠道组织结构完整，肠上皮层表面光滑平整，细胞形态保持完整且上皮细胞紧密附着于基底膜；与此同时CH组家蚕肠道上皮细胞组织则呈现出部分损伤的现象，有细胞破损和细胞核流出的情况，但上皮细胞仍与基底膜相连。相比之下，AC组家蚕肠道组织受到严重破坏，肠上皮细胞与基底膜出现明显分离，且细胞出现明显的碎裂现象(图2)。
2.3 氟暴露对昆虫肠道屏障和免疫谱的影响
通过逆转录实时定量聚合酶链式反应，探讨了氟暴露对家蚕肠道组织相关基因表达的影响。如图3所示，长期低浓度和短期高浓度氟暴露均对家蚕肠道组织的完整性产生了显著影响。与对照组(CK)相比，氟暴露后Toll信号通路中的关键调节基因Spz和Rel在CH组和AC组的表达分别下降至约5%和10%。此外，氟暴露还导致CH组和AC组的抗菌肽基因Att2、CecA、CecD和Leb1的表达显著下降，而CH组中的CecB6基因和AC组中的Lys基因表达量明显低于其他两组(图3)。这些结果表明氟暴露引起了昆虫宿主肠道免疫系统的紊乱，削弱了宿主的免疫功能，从而降低了昆虫对外界环境的适应能力。
2.4 氟暴露对昆虫肠道菌群的影响
采用16S rRNA基因扩增子测序技术，探讨了氟暴露对昆虫宿主肠道菌群组成的动态变化。实验结果显示，氟暴露后肠道菌群的主要优势菌门依次为芽孢杆菌门(Bacillota)、假单胞菌门(Pseudomonadota)、放线菌门(Actinobacteriota)、蓝藻门(Cyanobacteriota)和拟杆菌门(Bacteroidota) (图4A)。此外，肠道菌群中的前10个优势属细菌分别为肠球菌(Enterococcus)、未归类细菌(unclassified_f_Enterobacteriaceae)、肠杆菌(Enterobacteria)、谷氨酸杆菌(Glutamicibacter)、未归类细菌(norank_o_Chloroplast)、棒状杆菌(Corynebacterium)、葡萄球菌(Staphylococcus)、短状杆菌(Brachybacterium)、不动杆菌(Acinetobacter)和短杆菌(Brevibacterium)，其中以Enterococcus占据最优势地位(图4A)。氟暴露后，各组肠道菌群的α多样性未出现显著变化(图4B)。然而，PCoA分析结果表明，各组间肠道菌群的β多样性发生了显著改变，特别是AC组的肠道菌群结构呈现明显的趋同性。这表明短期高浓度氟暴露对昆虫宿主肠道菌群的异质性影响更为显著(图4C)。进一步的肠道菌群分析显示，与对照组相比，氟暴露导致肠道菌群显著失衡，且AC组的失衡指数最高(图4D)。这一结果表明，短期高浓度氟暴露对昆虫宿主肠道菌群的影响更为严重，导致肠道菌群紊乱的程度更大。
物种差异分析结果显示，导致各组肠道菌群差异的主要物种包括Glutamicibacter、Staphylococcus、Acinetobacter和Methylobacterium-Methylorubrum等，这些细菌在氟暴露后的相对丰度显著下降(图4E)。同时，线性判别分析(linear discriminant analysis effect, LEfSe)结果进一步证实，这4种属细菌是氟暴露后肠道菌群中的关键生物标志物(图4F)。综上所述，氟暴露实质性地影响了肠道菌群的组成结构。
2.5 氟暴露对昆虫肠道菌群潜在功能的影响
利用PICRUSt2软件对氟暴露后昆虫肠道菌群的功能进行了预测分析。结果显示，肠道菌群的主要功能类群包括碳水化合物转运与代谢(carbohydrate transport and metabolism)、氨基酸转运与代谢(amino acid transport and metabolism)和转录(transcription)等(图5A)。通过KEGG注释分析发现，氟暴露后AC组肠道菌群的metabolic pathways、biosynthesis of secondary metabolites、microbial metabolism in diverse environments、ABC transporters和biosynthesis of amino acids等途径的相对丰度明显升高(图5B)。此外，BugBase分析揭示，氟暴露后肠道菌群中potentially_pathogenic、facultatinvely_anaerobic、aerobic和forms_biofilms等表型发生了显著变化，其中AC组在这些表型的表现较其他两组显著下降(P<0.05)。这些结果体现了菌群代谢功能会伴随肠道微环境的改变而发生改变，进而说明氟暴露能实质性地影响肠道菌群的功能。这些结果还表明，氟暴露通过改变肠道菌群的结构，进而调节其代谢功能，最终影响昆虫宿主的生理状态。
3 讨论
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昆虫是地球化学循环和生态系统的重要组成部分。目前的研究指出，由于栖息地退化、农业生产和环境污染等人为因素，全球范围内昆虫的物种多样性、丰度和生物量呈现显著下降趋势[27]。近年研究发现，氟暴露能够引发多种高等生物疾病，其中胃肠道器官作为重要的代谢器官，受到的影响尤为显著。然而，不同氟暴露条件对昆虫宿主肠道微生态系统的影响尚不完全了解。目前，已知家蚕耐氟品种T6与氟敏感品种734在耐氟阈值上存在显著差异，使用这2种品种作为研究模型可能无法准确反映氟暴露对常见昆虫肠道微生态系统的影响[19-20]。因此，本研究选择了具有广泛代表性的家蚕生产用种‘菁松×皓月’，以探讨氟暴露对昆虫宿主肠道微生态系统的影响机制。简而言之，本研究结合多种生物学技术和方法，从多个角度揭示了氟暴露对昆虫宿主肠道微生态系统的损害机制。研究结果揭示，氟毒性与暴露剂量密切相关，且肠道微生态系统的破坏可能是导致昆虫宿主死亡的主要原因。
抗氧化系统是机体应对外界环境刺激引发氧化应激反应的一种自我保护机制，其中MDA含量可反映细胞膜的过氧化水平，而GSH则在维持免疫系统功能、抗氧化和解毒等方面发挥重要作用[28]。本研究表明，短期高浓度氟暴露后，家蚕肠道组织中的MDA含量显著升高，而GSH含量则显著下降，表明氟暴露会导致昆虫宿主肠道器官出现强烈的氧化应激反应。此外，CAT和SOD酶是机体抗氧化酶系统的关键酶，它们在维持细胞的稳定性和完整性方面发挥着重要作用[28]。本研究中，氟暴露后家蚕肠道组织中的CAT和SOD酶活性显著降低，表明不同浓度的氟暴露均能抑制昆虫宿主的抗氧化能力，从而破坏肠道细胞的完整性。病理学分析进一步揭示了氟暴露所引发的过度氧化应激反应对肠道上皮细胞造成的损伤程度。基础代谢酶如AChE、CarE、AKP/ALP和LDH在机体的生命代谢活动中发挥着重要作用。氟暴露对家蚕肠道组织中的这4种酶的活力产生了紊乱，尤其是短期高浓度氟暴露对这些酶的活力有显著抑制作用。已有研究表明，农药能够显著抑制AChE和CarE的酶活性，因此这2种酶被认为是检测杀虫剂毒性的生物标志物[29-30]。此外，Nasr等[29]发现，老鼠在遭受毒死蜱和阿维菌素暴露时LDH酶活性显著下降；Singh等[31]则指出，AKP/ALP酶在保护胃肠道器官方面具有重要作用，当肠道组织受损时，其酶活性会下降。上述结果表明氟暴露能够破坏昆虫宿主的多种生理基础代谢过程。
抗菌肽在昆虫免疫防御系统中发挥着清除病原体的作用，而Toll途径则是调节抗菌肽分泌的主要途径[32]。攻击素(attacin)、天蚕素(cecropin)和溶菌酶(lysozyme)是鳞翅目昆虫在病原体入侵后主要产生的抗菌肽[33]。荧光定量分析结果显示，氟暴露显著抑制了Toll途径关键调节基因的表达，同时也抑制了多种抗菌肽基因的表达。这表明氟暴露通过削弱昆虫宿主的免疫系统，降低了昆虫对外界环境的适应能力，这可能是导致昆虫种群数量下降的间接因素。
已知昆虫的肠道中栖息着大量复杂的微生物群落，这些微生物参与了昆虫的多种生理过程，包括发病机制和专性共生等相互作用[34]。本研究通过16S rRNA基因扩增子测序技术探讨了氟暴露对家蚕肠道内微生物群落组成及功能的影响。结果表明，氟暴露后肠道菌群中的谷氨酸杆菌(Glutamicibacter)、葡萄球菌(Staphylococcus)、不动杆菌(Acinetobacter)和甲基杆菌(Methylobacterium)等细菌表现出显著的相对丰度变化，这些细菌可能成为潜在的生物标志物。Feng等[36]研究表明，烟草蛾肠道中的Glutamicibacter能够降解植物毒素茄碱和卡茄碱，从而帮助宿主适应外界环境[35]。Staphylococcus在家蚕肠道内主要产生脂肪酶，有助于宿主抵抗BmNVP病毒侵染，以提高家蚕的生存率。此外，不动杆菌(Acinetobacter)和甲基杆菌(Methylobacterium)是家蚕肠道中的常见共生细菌，前者能产生酪蛋白酶、淀粉酶和脂肪酶，这些消化酶有助于家蚕对桑叶中营养成分的消化吸收[9,37]。因此，氟暴露可能通过降低这些潜在有益微生物的相对丰度导致家蚕肠道菌群失衡，进而破坏其肠道菌群的稳态。
4 结论
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氟暴露能够诱发昆虫宿主肠道组织的严重氧化应激反应，通过削弱抗氧化酶系统的活性，进一步破坏肠道组织的完整性。同时，这些抗氧化酶活性的下降还伴随着基础代谢酶活性的减弱，显著影响昆虫宿主的多种生理功能。氟暴露还会导致昆虫宿主免疫系统的紊乱，显著抑制其免疫功能，这可能是宿主生存率降低的关键因素。此外，氟暴露能改变昆虫宿主肠道菌群的结构组成，导致潜在有益微生物的数量减少，从而引发肠道菌群失衡。总之，通过削弱昆虫宿主的抗氧化能力、基础代谢能力、肠道屏障完整性、免疫功能以及肠道菌群结构，氟暴露实质性地破坏了肠道微生态系统的稳态，这可能是昆虫多样性和生物量下降的重要原因。本研究揭示了氟暴露对昆虫宿主毒害的潜在机制，并进一步强调了合理开发和保护环境以维持生态系统多样性与稳定性的重要意义。
基金
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  • 西南大学中央高校基本科研业务费专项资金(SWU-KR22028)
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2025年第65卷第10期
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文章信息
doi: 10.13343/j.cnki.wsxb.20250224
  • 接收时间：2025-03-20
  • 首发时间：2025-11-03
  • 出版时间：2025-09-04
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  • 收稿日期：2025-03-20
  • 录用日期：2025-04-23
基金
the Fundamental Research Funds for the Central Universities, Southwest University(SWU-KR22028)
西南大学中央高校基本科研业务费专项资金(SWU-KR22028)
作者信息
    1西南大学 蚕桑纺织与生物质科学学院，资源昆虫高效养殖与利用全国重点实验室，重庆
    2西南大学 西塔学院，重庆
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2种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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