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Article(id=1241342452251021326, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241342451043061769, articleNumber=null, orderNo=null, doi=10.20043/j.cnki.MPM.202311248, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1699804800000, receivedDateStr=2023-11-13, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1773888703643, onlineDateStr=2026-03-19, pubDate=1708790400000, pubDateStr=2024-02-25, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1773888703643, onlineIssueDateStr=2026-03-19, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1773888703643, creator=13701087609, updateTime=1773888703643, updator=13701087609, issue=Issue{id=1241342451043061769, tenantId=1146029695717560320, journalId=1227665162245664772, year='2024', volume='51', issue='4', pageStart='577', pageEnd='768', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1773888703356, creator=13701087609, updateTime=1773893026321, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1241360582939562716, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241342451043061769, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1241360582939562717, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241342451043061769, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=697, endPage=704, ext={EN=ArticleExt(id=1241342452544622612, articleId=1241342452251021326, tenantId=1146029695717560320, journalId=1227665162245664772, language=EN, title=Effects of high-fat diet in pre-pregnancy and pregnancy on gut microbiota of neonatal rats, columnId=1228016572065837304, journalTitle=Modern Preventive Medicine, columnName=Experimental Technology and Applications, runingTitle=null, highlight=null, articleAbstract=
Objective

To investigate the effects of high-fat diet in pre-pregnancy and pregnancy on gut microbiota of neonatal rats.

Methods

Twelve 3-week-old Specific Pathogen Free (SPF) female Sprague-dawley (SD) rats after one week of adaptive feeding were randomly divided into control group and high-fat diet group according to body weight. The rats were fed basal diet or high-fat diet until 12-week-old in pre-pregnancy, respectively, and then mated with SPF male SD rats of the same age. Pregnancy was determined the next day when vaginal plugs were observed or sperms were found by vaginal smears. Pregnant rats were kept in single cages and the diet in pregnancy was the same as pre-pregnancy. The postnatal day 0.5 (PD 0.5) neonatal rats were collected and the body weights were measured. Intestine of PD 0.5 neonatal rats were collected, intestinal weights were measured and intestinal coefficients were calculated. Histopathology and related genes detection of ileum and colon were performed. Total bacterial DNA of intestinal contents was extracted and the gut microbiota was analyzed by 16S rRNA sequencing. Data was analyzed by t test or Mann-Whitney U test.

Results

Compared with control group, there were no significant difference in the body weight, intestinal weight and intestinal coefficient in PD 0.5 neonatal rats of high-fat diet group(t=-0.682, P=0.499; t=0.269, P=0.790; t=0.674, P=0.506); there were no difference in intestinal histopathological changes; the gene expression level of Claudin-1, Lysozyme, Reg3γ (regenerating islet derived protein 3 gamma) and Alpha-defensin 5 of colon in PD 0.5 neonatal rats of high-fat diet group were increased significantly(t=-3.136，P=0.011; t=-3.303, P=0.019; t=-3.093, P=0.011; t=-3.575, P=0.005); there were no significant difference in α diversity and β diversity of gut microbiota(t=-1.407, P=0.190; t=-1.410, P=0.189; t=-2.017, P=0.071; U=6.000, P=0.055; F=1.030，P=0.141); the abundance of Ruminococcus, Phascolarctobacterium, Lachnospiracea_incertae_sedis, Veillonella and Flavobacterium and Bacteroides_sp._SLC1-38 increased significantly(U=3.500, P=0.013; U=7.000, P＝0.050; U=6.000, P=0.022; U=6.000, P=0.022; U=7.000, P＝0.050; U=3.000, P=0.007). The Linear discriminant analysis Effect Size (LEfSe) analysis found that Escherella/Shigella, Ruminococcus, Phascolarctobacterium, Lachnospiracea_incertae_sedis and Bacteroides_SP._SLC1-38 were bacteria with effects on the differences in high-fat diet group greater than the set value.

Conclusion

High-fat diet in pre-pregnancy and pregnancy increased the abundance of metabolically related bacteria and pathogenic bacteria in the gut of PD 0.5 neonatal rats.

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目的

探讨孕前和孕期高脂饲料喂养对新生大鼠肠道菌群的影响。

方法

12只3周龄无特定病原体（Specific Pathogen Free，SPF）级雌性Sprague-dawley（SD）大鼠，适应性喂养一周后，按体重随机分为对照组与高脂组，孕前分别用基础饲料与高脂饲料喂养至12周龄，与同周龄SPF级雄性SD大鼠合笼，次日观察到阴道栓或阴道涂片中发现精子后，判定受孕。孕鼠单笼饲养，孕期的饲料与孕前相同。收集出生后第0.5天（postnatal day 0.5，PD 0.5）仔鼠，称量体重，采集肠道组织并称量质量，计算肠道系数；进行回肠和结肠组织病理和相关基因检测；提取肠道内容物的细菌总DNA，通过16S rRNA测序分析肠道菌群。采用t检验或Mann-Whitney U检验分析数据。

结果

与对照组相比，高脂组PD 0.5仔鼠体重、肠道质量、肠道系数无显著改变（t=-0.682, P=0.499; t=0.269, P=0.790; t=0.674, P=0.506）；肠道病理形态无改变; 结肠闭合蛋白-1（Claudin-1）、溶菌酶（Lysozyme）、再生胰岛衍生蛋白3伽马（regenerating islet derived protein 3 gamma，Reg3γ）和α-防御素5（Alpha-defensin 5）的基因表达水平显著增加（t=-3.136，P=0.011; t=-3.303, P=0.019；t=-3.093, P=0.011；t=-3.575, P=0.005）；肠道菌群的α多样性和β多样性无显著改变（t=-1.407, P=0.190；t=-1.410, P=0.189；t=-2.017, P=0.071；U=6.000, P=0.055；F=1.030，P=0.141）；肠道瘤胃球菌属、考拉杆菌属、Lachnospiracea_incertae_sedis、韦荣氏球菌属、黄杆菌属和Bacteroides_sp._SLC1-38的丰度显著增加（U=3.500, P=0.013；U=7.000, P＝0.050；U=6.000, P=0.022；U=6.000, P=0.022；U=7.000, P＝0.050; U=3.000, P=0.007）；线性判别分析效应量（Linear discriminant analysis Effect Size，LEfSe）分析表明高脂组中对差异影响贡献较大的物种有埃希氏菌属/志贺氏菌属、瘤胃球菌属、考拉杆菌属、Lachnospiracea_incertae_sedis和Bacteroides_SP._SLC1-38。

结论

孕前和孕期高脂饲料喂养导致PD 0.5仔鼠肠道代谢相关菌和致病菌的丰度增加。

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余焕玲，E-mail：
, copyrightStatement=本刊刊出的所有文章不代表中华预防医学会和本刊编委会的观点，除非特别声明。, copyrightOwner=中华预防医学会和四川大学华西公共卫生学院, extLink=null, articleAbsUrl=null, sourceXml=eualju4J7u7eszD17rcx6w==, magXml=SNTlR76Lq5a4NU5m8etqPQ==, pdfUrl=null, pdf=0fEN3F0m+xl4q1rNtS/cpg==, pdfFileSize=2807023, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=WDT2ZcwPfwsPNN9jexQ3SQ==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=l+PCITxSQtkzUX3WbC8/rQ==, mapNumber=null, authorCompany=null, fund=null, authors=

胡卓（1999—），男，硕士在读，研究方向：营养与疾病

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胡卓（1999—），男，硕士在读，研究方向：营养与疾病

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胡卓（1999—），男，硕士在读，研究方向：营养与疾病

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PLOS One, 2015, 10(5): e0126931., articleTitle=Changes in gut microbiota in rats fed a high fat diet correlate with obesity-associated metabolic parameters, refAbstract=null), Reference(id=1241342470013899583, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, doi=null, pmid=null, pmcid=null, year=2019, volume=64, issue=null, pageStart=228, pageEnd=236, url=null, language=null, rfNumber=[22], rfOrder=22, authorNames=Mayengbam S, Lambert JE, Parnell JA, journalName=Journal of Nutritional Biochemistry, refType=null, unstructuredReference=Mayengbam S, Lambert JE, Parnell JA, et al. Impact of dietary fiber supplementation on modulating microbiota-host-metabolic axes in obesity[J]. 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Journal of Nutrition, 2017, 147(1): 20-28., articleTitle=Early-Life sugar consumption affects the rat microbiome independently of obesity, refAbstract=null), Reference(id=1241342470273946449, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, doi=null, pmid=null, pmcid=null, year=2021, volume=79, issue=6, pageStart=709, pageEnd=725, url=null, language=null, rfNumber=[24], rfOrder=24, authorNames=Gawlińska K, Gawliński D, Filip M, journalName=Nutrition Reviews, refType=null, unstructuredReference=Gawlińska K, Gawliński D, Filip M, et al. Relationship of maternal high-fat diet during pregnancy and lactation to offspring health[J]. 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Mammalian Genome, 2018, 29(7/8): 558-576., articleTitle=Enterobacteria and host resistance to infection, refAbstract=null), Reference(id=1241342472027165541, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, doi=null, pmid=null, pmcid=null, year=2023, volume=20, issue=7, pageStart=417, pageEnd=432, url=null, language=null, rfNumber=[27], rfOrder=27, authorNames=Horowitz A, Chanez-Paredes SD, Haest X, journalName=Nature Reviews Gastroenterology & Hepatology, refType=null, unstructuredReference=Horowitz A, Chanez-Paredes SD, Haest X, et al. Paracellular permeability and tight junction regulation in gut health and disease[J]. 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Gut, 2020, 69(12): 2232-2243., articleTitle=Mucus barrier, mucins and gut microbiota: the expected slimy partners?, refAbstract=null), Reference(id=1241342472270435185, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, doi=null, pmid=null, pmcid=null, year=2020, volume=38, issue=null, pageStart=23, pageEnd=48, url=null, language=null, rfNumber=[29], rfOrder=29, authorNames=Kayama H, Okumura R, Takeda K, journalName=Annual Review of Immunology, refType=null, unstructuredReference=Kayama H, Okumura R, Takeda K. Interaction between the microbiota, epithelia, and immune cells in the intestine[J]. Annual Review of Immunology, 2020, 38: 23-48., articleTitle=Interaction between the microbiota, epithelia, and immune cells in the intestine, refAbstract=null), Reference(id=1241342472362709874, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, doi=null, pmid=null, pmcid=null, year=2022, volume=46, issue=5, pageStart=701, pageEnd=710, url=null, language=null, rfNumber=[30], rfOrder=30, authorNames=Barreto E Barreto L, Rattes IC, da Costa AV, journalName=Cell Biology International, refType=null, unstructuredReference=Barreto E Barreto L, Rattes IC, da Costa AV, et al. Paneth cells and their multiple functions[J]. Cell Biology International, 2022, 46(5): 701-710., articleTitle=Paneth cells and their multiple functions, refAbstract=null)], funds=[Fund(id=1241342465882509980, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, awardId=KZ202210025039, language=CN, fundingSource=北京市教育委员会科技/社科计划项目(KZ202210025039), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1241342456449519747, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, xref=null, ext=[AuthorCompanyExt(id=1241342456457908356, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, companyId=1241342456449519747, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=Department of Nutrition and Food Hygiene, College of Public Health, Capital Medical University, Beijing 100069, China), AuthorCompanyExt(id=1241342456466296965, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, companyId=1241342456449519747, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=首都医科大学公共卫生学院营养与食品卫生学系，北京 100069)])], figs=[ArticleFig(id=1241342463613391314, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=EN, label=Fig.1, caption=Body weight, intestinal weight and intestinal coefficient of PD 0.5 neonatal rats, figureFileSmall=B8a4K6MoajzVJrkdZ525vg==, figureFileBig=WDT2ZcwPfwsPNN9jexQ3SQ==, tableContent=null), ArticleFig(id=1241342463743414750, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=CN, label=图1, caption=PD 0.5仔鼠的体重、肠道质量和肠道系数

注：A:体重；B：肠道质量；C：肠道系数。n=20。

, figureFileSmall=B8a4K6MoajzVJrkdZ525vg==, figureFileBig=WDT2ZcwPfwsPNN9jexQ3SQ==, tableContent=null), ArticleFig(id=1241342463978295796, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=EN, label=Fig.2, caption=Histopathology of intestinal tissues of PD 0.5neonatal rats, figureFileSmall=/LkU2qtq0fR9dKZEVjZvpg==, figureFileBig=A4QHdekpj5+FpI9T4j8mPg==, tableContent=null), ArticleFig(id=1241342464062181889, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=CN, label=图2, caption=PD 0.5仔鼠肠道组织病理形态

注：A: HE染色（×200）; B: AB-PAS染色（×200）; C: 荧光桃红染色（×200）。

, figureFileSmall=/LkU2qtq0fR9dKZEVjZvpg==, figureFileBig=A4QHdekpj5+FpI9T4j8mPg==, tableContent=null), ArticleFig(id=1241342464171233803, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=EN, label=Fig.3, caption=Difference analysis of villus height, crypt depth, goblet cell number and Paneth cell number of intestinal tissues of PD 0.5 neonatal rats, figureFileSmall=rad9i93jgrmJAsm8CdvRLA==, figureFileBig=Ao1f78jeazkP8fBX8jd7fA==, tableContent=null), ArticleFig(id=1241342464288674330, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=CN, label=图3, caption=PD 0.5仔鼠肠道组织绒毛高度、隐窝深度、杯状细胞数量和潘氏细胞数量差异分析

注：A、C、E：回肠组织绒毛高度、杯状细胞数量、潘氏细胞数量；B、D：结肠组织隐窝深度、杯状细胞数量。回肠组织n=4，结肠组织n=3。

, figureFileSmall=rad9i93jgrmJAsm8CdvRLA==, figureFileBig=Ao1f78jeazkP8fBX8jd7fA==, tableContent=null), ArticleFig(id=1241342464435474983, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=EN, label=Fig.4, caption=The mRNA expression level ofOccludin, ZO-1, Claudin-1, MUC2 of intestinal tissues of PD 0.5 neonatal rats, figureFileSmall=M0i7akR5VgBmrDY1E2Ktww==, figureFileBig=SaAGlc4RD/L0WWwbygKHiQ==, tableContent=null), ArticleFig(id=1241342464586469942, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=CN, label=图4, caption=PD 0.5仔鼠肠道Occludin, ZO-1, Claudin-1, MUC2的mRNA水平

注：A-D:回肠组织Occludin, ZO-1, Claudin-1, MUC2表达水平；E-H：结肠组织Occludin, ZO-1, Claudin-1, MUC2表达水平。n=6,*P<0.05,下同。

, figureFileSmall=M0i7akR5VgBmrDY1E2Ktww==, figureFileBig=SaAGlc4RD/L0WWwbygKHiQ==, tableContent=null), ArticleFig(id=1241342464695521860, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=EN, label=Fig.5, caption=The mRNA expression level of antimicrobial peptides of intestinal tissues of PD 0.5 neonatal rats, figureFileSmall=KIb58VwD42oIx0dtl9qVTg==, figureFileBig=kj0cg6j9NUX8Eyw3MMGFWg==, tableContent=null), ArticleFig(id=1241342464804573772, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=CN, label=图5, caption=PD 0.5仔鼠肠道抗菌肽的mRNA水平

注：A-C:回肠组织Lysozyme, Reg3γ, Alpha-defensin 5表达水平；D-F：结肠组织Lysozyme，Reg3γ, Alpha-defensin 5表达水平。

, figureFileSmall=KIb58VwD42oIx0dtl9qVTg==, figureFileBig=kj0cg6j9NUX8Eyw3MMGFWg==, tableContent=null), ArticleFig(id=1241342464905237076, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=EN, label=Fig.6, caption=Diversity analysis ofgut microbiota, figureFileSmall=dBsBwbRscXKEOsACshxm3g==, figureFileBig=GbDdgimwybpPG/CXNRf5Xg==, tableContent=null), ArticleFig(id=1241342465022677597, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=CN, label=图6, caption=肠道菌群多样性分析

注：A：韦恩图；B:α多样性指数；C：PCoA图。

, figureFileSmall=dBsBwbRscXKEOsACshxm3g==, figureFileBig=GbDdgimwybpPG/CXNRf5Xg==, tableContent=null), ArticleFig(id=1241342465140118118, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=EN, label=Fig.7, caption=Composition anddifference analysis of gut microbiota, figureFileSmall=xXDKdb7L3BZlRlnAmIN2Lw==, figureFileBig=KkdPx9tIzadFed1QL/Cfag==, tableContent=null), ArticleFig(id=1241342465244975730, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=CN, label=图7, caption=肠道菌群组成和差异分析

注：A：门水平物种组成柱状图；B：属水平物种组成柱状图; C：差异肠道菌群热图；D：LDA条形图。Unassigned: 分类学比对时在设定的置信阈值以下，No_Rank: 在门/属上没有明确的分类信息或分类名称。

, figureFileSmall=xXDKdb7L3BZlRlnAmIN2Lw==, figureFileBig=KkdPx9tIzadFed1QL/Cfag==, tableContent=null), ArticleFig(id=1241342465349833338, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=EN, label=Table 1, caption=

The energy supply ratios of macronutrients and energy densities of the diets

, figureFileSmall=null, figureFileBig=null, tableContent=
供能比基础饲料高脂饲料
碳水化合物（%）7020
蛋白质（%）2020
脂肪（%）1060
能量（kcal/g）3.855.24
), ArticleFig(id=1241342465492439681, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=CN, label=表1, caption=

饲料中的宏量营养素供能比和能量密度

, figureFileSmall=null, figureFileBig=null, tableContent=
供能比基础饲料高脂饲料
碳水化合物（%）7020
蛋白质（%）2020
脂肪（%）1060
能量（kcal/g）3.855.24
), ArticleFig(id=1241342465605685898, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=EN, label=Table 2, caption=

Primer sequences of reference gene and target genes

, figureFileSmall=null, figureFileBig=null, tableContent=
基因序列(5’ to 3’)
β-actinF: GGTCAGGTCATCACTATCGGCAATG
R: CAGCACTGTGTTGGCATAGAGGTC
OccludinF: CAACGGCAAAGTGAATGGCAAGAG
R: TCATCCACGGACAAGGTCAGAGG
ZO-1F: CAAGCCAGTCCATTCTCAGAGTCAG
R: TCCATAGCATCAGTTTCGGGTTTCC
Claudin-1F: GTGTGACAGCGGCGAAGGAAG
R: ACTCAGTGGCAAGCAGCAGTTC
MUC2F: CTCACCAACCACCTCAACCACTTC
R: TCCAGAATCCAGCCAGCCAGTC
LysozymeF: CCGCACAGTCTCACCACACAC
R: GTTCAGGCAGTCTCAGTTCTCATCC
Reg3γF: AGGTGAAGATGCCAAGGAAGATGTG
R: GATCCACTGAGCACAGACACAAGG
Alpha-defensin 5F: ACTCTGCTTACCGCCCTTCTCC
R: GTCACGCCTGCCTTCACATCTG
), ArticleFig(id=1241342465697960595, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241342452251021326, language=CN, label=表2, caption=

内参基因及目的基因引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
基因序列(5’ to 3’)
β-actinF: GGTCAGGTCATCACTATCGGCAATG
R: CAGCACTGTGTTGGCATAGAGGTC
OccludinF: CAACGGCAAAGTGAATGGCAAGAG
R: TCATCCACGGACAAGGTCAGAGG
ZO-1F: CAAGCCAGTCCATTCTCAGAGTCAG
R: TCCATAGCATCAGTTTCGGGTTTCC
Claudin-1F: GTGTGACAGCGGCGAAGGAAG
R: ACTCAGTGGCAAGCAGCAGTTC
MUC2F: CTCACCAACCACCTCAACCACTTC
R: TCCAGAATCCAGCCAGCCAGTC
LysozymeF: CCGCACAGTCTCACCACACAC
R: GTTCAGGCAGTCTCAGTTCTCATCC
Reg3γF: AGGTGAAGATGCCAAGGAAGATGTG
R: GATCCACTGAGCACAGACACAAGG
Alpha-defensin 5F: ACTCTGCTTACCGCCCTTCTCC
R: GTCACGCCTGCCTTCACATCTG
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孕前和孕期高脂饲料喂养对新生大鼠肠道菌群的影响
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胡卓 , 杨倩 , 魏宇辰 , 蔡夏夏 , 党秦豫 , 朱砚荻 , 张亚迪 , 陈朝阳 , 余焕玲
现代预防医学 | 实验技术及其应用 2024,51(4): 697-704
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现代预防医学 | 实验技术及其应用 2024, 51(4): 697-704
孕前和孕期高脂饲料喂养对新生大鼠肠道菌群的影响
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胡卓, 杨倩, 魏宇辰, 蔡夏夏, 党秦豫, 朱砚荻, 张亚迪, 陈朝阳, 余焕玲
作者信息
  • 首都医科大学公共卫生学院营养与食品卫生学系，北京 100069

    • 胡卓（1999—），男，硕士在读，研究方向：营养与疾病

通讯作者:

余焕玲，E-mail：
Effects of high-fat diet in pre-pregnancy and pregnancy on gut microbiota of neonatal rats
Zhuo HU, Qian YANG, Yu-chen WEI, Xia-xia CAI, Qin-yu DANG, Yan-di ZHU, Ya-di ZHANG, Zhao-yang CHEN, Huan-ling YU
Affiliations
  • Department of Nutrition and Food Hygiene, College of Public Health, Capital Medical University, Beijing 100069, China
出版时间: 2024-02-25 doi: 10.20043/j.cnki.MPM.202311248
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摘要
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目的

探讨孕前和孕期高脂饲料喂养对新生大鼠肠道菌群的影响。

方法

12只3周龄无特定病原体（Specific Pathogen Free，SPF）级雌性Sprague-dawley（SD）大鼠，适应性喂养一周后，按体重随机分为对照组与高脂组，孕前分别用基础饲料与高脂饲料喂养至12周龄，与同周龄SPF级雄性SD大鼠合笼，次日观察到阴道栓或阴道涂片中发现精子后，判定受孕。孕鼠单笼饲养，孕期的饲料与孕前相同。收集出生后第0.5天（postnatal day 0.5，PD 0.5）仔鼠，称量体重，采集肠道组织并称量质量，计算肠道系数；进行回肠和结肠组织病理和相关基因检测；提取肠道内容物的细菌总DNA，通过16S rRNA测序分析肠道菌群。采用t检验或Mann-Whitney U检验分析数据。

结果

与对照组相比，高脂组PD 0.5仔鼠体重、肠道质量、肠道系数无显著改变（t=-0.682, P=0.499; t=0.269, P=0.790; t=0.674, P=0.506）；肠道病理形态无改变; 结肠闭合蛋白-1（Claudin-1）、溶菌酶（Lysozyme）、再生胰岛衍生蛋白3伽马（regenerating islet derived protein 3 gamma，Reg3γ）和α-防御素5（Alpha-defensin 5）的基因表达水平显著增加（t=-3.136，P=0.011; t=-3.303, P=0.019；t=-3.093, P=0.011；t=-3.575, P=0.005）；肠道菌群的α多样性和β多样性无显著改变（t=-1.407, P=0.190；t=-1.410, P=0.189；t=-2.017, P=0.071；U=6.000, P=0.055；F=1.030，P=0.141）；肠道瘤胃球菌属、考拉杆菌属、Lachnospiracea_incertae_sedis、韦荣氏球菌属、黄杆菌属和Bacteroides_sp._SLC1-38的丰度显著增加（U=3.500, P=0.013；U=7.000, P＝0.050；U=6.000, P=0.022；U=6.000, P=0.022；U=7.000, P＝0.050; U=3.000, P=0.007）；线性判别分析效应量（Linear discriminant analysis Effect Size，LEfSe）分析表明高脂组中对差异影响贡献较大的物种有埃希氏菌属/志贺氏菌属、瘤胃球菌属、考拉杆菌属、Lachnospiracea_incertae_sedis和Bacteroides_SP._SLC1-38。

结论

孕前和孕期高脂饲料喂养导致PD 0.5仔鼠肠道代谢相关菌和致病菌的丰度增加。

高脂饮食  /  子代  /  肠道菌群  /  16S rRNA
Objective

To investigate the effects of high-fat diet in pre-pregnancy and pregnancy on gut microbiota of neonatal rats.

Methods

Twelve 3-week-old Specific Pathogen Free (SPF) female Sprague-dawley (SD) rats after one week of adaptive feeding were randomly divided into control group and high-fat diet group according to body weight. The rats were fed basal diet or high-fat diet until 12-week-old in pre-pregnancy, respectively, and then mated with SPF male SD rats of the same age. Pregnancy was determined the next day when vaginal plugs were observed or sperms were found by vaginal smears. Pregnant rats were kept in single cages and the diet in pregnancy was the same as pre-pregnancy. The postnatal day 0.5 (PD 0.5) neonatal rats were collected and the body weights were measured. Intestine of PD 0.5 neonatal rats were collected, intestinal weights were measured and intestinal coefficients were calculated. Histopathology and related genes detection of ileum and colon were performed. Total bacterial DNA of intestinal contents was extracted and the gut microbiota was analyzed by 16S rRNA sequencing. Data was analyzed by t test or Mann-Whitney U test.

Results

Compared with control group, there were no significant difference in the body weight, intestinal weight and intestinal coefficient in PD 0.5 neonatal rats of high-fat diet group(t=-0.682, P=0.499; t=0.269, P=0.790; t=0.674, P=0.506); there were no difference in intestinal histopathological changes; the gene expression level of Claudin-1, Lysozyme, Reg3γ (regenerating islet derived protein 3 gamma) and Alpha-defensin 5 of colon in PD 0.5 neonatal rats of high-fat diet group were increased significantly(t=-3.136，P=0.011; t=-3.303, P=0.019; t=-3.093, P=0.011; t=-3.575, P=0.005); there were no significant difference in α diversity and β diversity of gut microbiota(t=-1.407, P=0.190; t=-1.410, P=0.189; t=-2.017, P=0.071; U=6.000, P=0.055; F=1.030，P=0.141); the abundance of Ruminococcus, Phascolarctobacterium, Lachnospiracea_incertae_sedis, Veillonella and Flavobacterium and Bacteroides_sp._SLC1-38 increased significantly(U=3.500, P=0.013; U=7.000, P＝0.050; U=6.000, P=0.022; U=6.000, P=0.022; U=7.000, P＝0.050; U=3.000, P=0.007). The Linear discriminant analysis Effect Size (LEfSe) analysis found that Escherella/Shigella, Ruminococcus, Phascolarctobacterium, Lachnospiracea_incertae_sedis and Bacteroides_SP._SLC1-38 were bacteria with effects on the differences in high-fat diet group greater than the set value.

Conclusion

High-fat diet in pre-pregnancy and pregnancy increased the abundance of metabolically related bacteria and pathogenic bacteria in the gut of PD 0.5 neonatal rats.

High-fat diet  /  Offspring  /  Gut microbiota  /  16s rRNA
胡卓, 杨倩, 魏宇辰, 蔡夏夏, 党秦豫, 朱砚荻, 张亚迪, 陈朝阳, 余焕玲. 孕前和孕期高脂饲料喂养对新生大鼠肠道菌群的影响. 现代预防医学, 2024 , 51 (4) : 697 -704 . DOI: 10.20043/j.cnki.MPM.202311248
Zhuo HU, Qian YANG, Yu-chen WEI, Xia-xia CAI, Qin-yu DANG, Yan-di ZHU, Ya-di ZHANG, Zhao-yang CHEN, Huan-ling YU. Effects of high-fat diet in pre-pregnancy and pregnancy on gut microbiota of neonatal rats[J]. Modern Preventive Medicine, 2024 , 51 (4) : 697 -704 . DOI: 10.20043/j.cnki.MPM.202311248
正文
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肠道菌群是一个由多达100万亿个微生物组成的复杂群落，对宿主的生长发育、营养吸收与代谢、免疫屏障等具有重要作用[1-2]。新生儿肠道菌群的定植始于分娩，是一个复杂微生物群落从头组装的动态过程，自然分娩时，来自母亲阴道和粪便的菌群构成了子代肠道菌群定植的基础[3-5]。肠道菌群初始定植的改变会对未来的定植产生影响,与后续生命过程中的心血管疾病、肥胖和神经系统疾病等的发生和发展相关[6-10]。
母亲高脂饮食会影响子代肠道菌群。Ma等人发现孕期和哺乳期高脂饲料喂养的日本猕猴，其1岁子代的肠道弯曲杆菌属、螺杆菌属丰度降低，瘤胃球菌属和戴阿利斯特菌属的丰度增加[11]；Myles等人发现孕期高脂饲料喂养的小鼠，断乳子代的肠道菌群α多样性降低，梭菌目和毛螺菌科的丰度增加[12]。上述研究提示孕期高脂饮食与子代肠道菌群的多样性以及某些细菌的丰度存在关联。饮食是影响肠道菌群组成的重要环境因素[13-14]，随着生活水平的日益改善，我国居民膳食逐渐呈现高能量、高脂肪、高蛋白质、低膳食纤维的西方膳食模式特点，脂肪的供能比显著增加[15]。目前，虽然有研究发现了孕前和孕期高脂饮食与子代肠道菌群之间的关联，但是，这种关联是否始于肠道微生物的初始定植，则不清楚。为此，本研究于孕前和孕期连续饲喂Sprague-dawley（SD）大鼠高脂饲料，观察出生后第0.5天（postnatal day 0.5，PD 0.5）仔鼠的肠道病理形态、屏障功能和肠道菌群，探讨孕前和孕期高脂饲料喂养对PD 0.5子代肠道菌群的影响。
1　材料与方法
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1.1　实验动物与分组
12只3周龄无特定病原体（Specific Pathogen Free，SPF）级雌性Sprague-dawley（SD）大鼠，购自北京维通利华实验动物技术有限公司，饲养于首都医科大学实验动物中心，环境温度为（20±2）°C、光/暗各12 h，自由饮水和摄食。适应性喂养一周后，按体重随机分为对照组与高脂组，孕前分别用基础饲料与高脂饲料喂养至12周龄，与同周龄SPF级雄性SD大鼠以3：1的比例合笼过夜。次日，若观察到阴道栓或阴道涂片中发现精子，判定为受孕成功。孕鼠单笼饲养，孕期的饲料与孕前相同。收集PD 0.5仔鼠，每组分别随机选取20只进行称重，用300 mg/kg三溴乙醇进行麻醉，解剖肠道组织后称量质量，计算肠道系数，分离回肠组织和结肠组织。分别提取回肠组织和结肠组织的mRNA；无菌环境采集肠道的全部内容物，提取细菌总DNA，用于后续实验。所有的检测样品均未进行混合，各个检测指标中每组PD 0.5仔鼠分别来自2~3只不同的母鼠。实验操作得到首都医科大学医学伦理委员会批准（伦理号：AEI-2021-136）。
1.2　动物饲料
饲料购自北京华阜康生物科技股份有限公司，基础饲料（型号：D12450B）和高脂饲料（型号：D12492）宏量营养素的供能比和能量密度见表1。
1.3　肠道组织病理
取PD 0.5仔鼠回肠和结肠组织，经4%多聚甲醛溶液固定、脱水、石蜡包埋、切片、染色和封片后，在光学显微镜下观察肠道病理形态。用苏木精-伊红（Hematoxylin-Eosin，HE）染色观察回肠和结肠组织形态，并测量绒毛长度和隐窝深度；用阿尔新蓝/高碘酸雪夫（Alcian Blue-Periodic Acid Schiff，AB-PAS）染色观察回肠和结肠中的杯状细胞，并进行计数；用荧光桃红染色观察回肠中的潘氏细胞，并进行计数。每个样本组织切片取5个完整绒毛或隐窝视野。
1.4　定量聚合酶链反应
使用磁珠法组织总RNA提取试剂盒（天根生化科技有限公司）分别从PD 0.5仔鼠的回肠和结肠组织提取RNA，按照RNA逆转录试剂盒（赛默飞生物公司）要求将RNA反转录成c DNA。按照 SYBR试剂盒（近岸蛋白质科技股份有限公司）说明书配置qPCR反应液并设置扩增条件。引物由生工生物工程（上海）股份有限公司合成，序列见表2。用2-ΔΔCt表示目的基因的相对表达量。
1.5　肠道菌群分析
无菌环境收集PD 0.5仔鼠肠道的全部内容物，提取肠道菌群的总DNA，琼脂糖凝胶电泳检测基因组DNA的完整性：电泳条带清晰可见，无明显降解；Nanodrop 2000检测基因组DNA质量：浓度≥20 ng/μl，总量≥500 ng，OD260/280=1.8~2.0。对于合格的样本检测区域进行高保真PCR扩增，扩增引物选定的检测区域为V3-V4区域。扩增后产物琼脂糖凝胶电泳检测，应用核酸纯化磁珠对扩增产物进行纯化，得到样本的原始文库。文库检测合格后，采用NovaSeq 6000平台，SP-Xp（PE250）的双端测序策略对文库进行测序，后续进行生物信息学分析。使用QIIME2的DADA2插件进行质控后直接生成扩增序列变体（amplicon sequence variant，ASV）和操作分类单元（Operational Taxonomic Unit，OTU）。使用QIIME2软件对ASV/OTU序列进行物种注释。注释方法：classify-sklearn。对ASV/OTU分类学表进行各分类水平物种注释情况统计。
用韦恩图展示每组样本中特有的以及组间共有的ASV /OTU。分析ACE指数、Chao1 指数、shannon指数、Simpson指数等展示肠道菌群的α多样性。主坐标分析（Principal Coordinate Analysis，PCoA）检测β多样性，同时使用基于Bray-curtis 距离的ADONIS分析检验组间β多样性的差异。柱状图反映两组门、属水平上的物种组成。t检验或Mann-Whitney U检验分析组间差异的物种，检验水准α=0.05。线性判别分析效应量（Linear discriminant analysis Effect Size，LEfSe）分析筛选最可能解释组间差异的物种，线性判别分析（Linear discriminant analysis，LDA）评估每个差异显著的物种的效应值，以LDA score>3作为差异显著性阈值。
1.6　统计学处理
利用SPSS 26.0软件和在线工具ImageGP[16]对数据进行处理和分析。计量资料以（）表示。两组间数据比较采用t检验或Mann-Whitney U检验，检验水准α=0.05。
2　结果
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2.1　孕前和孕期高脂饲料喂养对PD 0.5仔鼠生长发育的影响
结果显示，PD 0.5仔鼠的体重、肠道质量以及肠道系数在对照组和高脂组之间无统计学差异（t=-0.682, P=0.499; t=0.269, P=0.790; t=0.674, P=0.506）（见图1）。
2.2　孕前和孕期高脂饲料喂养对PD 0.5仔鼠肠道形态的影响
HE染色结果显示，对照组和高脂组PD 0.5仔鼠肠道绒毛和隐窝表面单层柱状细胞均排列紧密，细胞形态正常（见图2A），统计分析发现回肠绒毛高度和结肠隐窝深度在两组间无统计学差异（t=-1.827, P=0.076; t=0.126, P=0.901）（见图3A和3B）。AB-PAS染色将杯状细胞染为深蓝色（见图2B），统计分析发现，回肠和结肠内杯状细胞数量在两组间无统计学差异（t=-0.464, P=0.646; t=0.137, P=0.892）（见图3C和3D）。荧光桃红染色将潘氏细胞染为品红色（见图2C），统计分析发现，回肠潘氏细胞数量在两组间无统计学差异（U=164.500，P=0.327）（见图3E）。
2.3　孕前和孕期高脂饲料喂养对PD 0.5仔鼠肠道紧密连接蛋白和黏蛋白mRNA表达水平的影响
肠道紧密连接蛋白和黏蛋白与肠道屏障功能密切相关，阻止微生物侵入肠道上皮。与对照组相比，高脂组PD 0.5仔鼠回肠组织中咬合蛋白（Occludin）、闭锁小带蛋白-1（zona occludens-1，ZO-1）、闭合蛋白-1（Claudin-1）和黏蛋白2（Mucin 2，MUC2）的基因表达水平无显著改变（t=-0.190, P=0.853；t=1.068, P＝0.311；t=0.207, P=0.840；t=1.003, P=0.340）。与对照组相比，高脂组PD 0.5仔鼠结肠组织中Occludin、ZO-1和MUC2基因的表达水平的无显著改变（U=13.000, P=0.423；t=-0.527, P=0.610；U=8.000, P=0.109）；Claudin-1基因的表达水平显著升高（t=-3.136，P=0.011）（见图4）。
2.4　孕前和孕期高脂饲料喂养对PD 0.5仔鼠肠道抗菌肽mRNA表达水平的影响
肠道抗菌肽对抵御微生物和防止感染至关重要。与对照组相比，高脂组PD 0.5仔鼠回肠溶菌酶（Lysozyme）、再生胰岛衍生蛋白3伽马（regenerating islet derived protein 3 gamma，Reg3γ）和α-防御素5（Alpha-defensin 5）的基因表达水平无显著改变（t=-0.465, P=0.652；t=-0.118, P=0.908；t=0.183, P=0.859）；结肠Lysozyme、Reg3γ和Alpha-defensin 5基因的表达水平显著升高（t=-3.303, P=0.019；t=-3.093, P=0.011；t=-3.575, P=0.005）（见图5）。
2.5　孕前和孕期高脂饲料喂养对PD 0.5仔鼠肠道菌群的影响
2.5.1　肠道菌群多样性
为了研究孕前和孕期高脂饲料喂养对PD 0.5仔鼠肠道菌群结构的影响，我们分析了肠道菌群ASV /OTU数量，α多样性和β多样性。结果显示，对照组特有的ASV /OTU为 2068种，高脂组特有的ASV /OTU为2878种，两组共有的ASV /OTU为396种（见图6A）。我们分别用ACE和Chao1指数反映肠道菌群的丰富度，用Shannon和Simpson指数反映肠道菌群的多样性，结果显示两组之间无统计学差异（t=-1.407, P=0.190；t=-1.410, P=0.189；t=-2.017, P=0.071；U=6.000, P=0.055）（见图6B）。用PCoA和基于Bray-curtis距离的ADONIS分析反映肠道菌群的β多样性，结果显示第一主成分 PCoA1和第二主成分PCoA2对区分两组的贡献度分别为10.6%和10.1%，两组间β多样性无统计学差异（F=1.030，P=0.141）（见图6C）。
2.5.2　肠道菌群组成和差异
在门水平上，PD 0.5仔鼠肠道的主要优势菌群为厚壁菌门，变形菌门，拟杆菌门和放线菌门等（见图7A），各菌门的差异均无统计学意义（均P>0.05）。
在属水平上，PD 0.5仔鼠肠道的主要优势菌群为埃希氏菌属/志贺氏菌属，拟杆菌属，葡萄球菌属和乳杆菌属等（见图7B）。高脂组PD 0.5仔鼠肠道瘤胃球菌属、考拉杆菌属、Lachnospiracea_incertae_sedis、韦荣氏球菌属和黄杆菌属的丰度显著高于对照组（U=3.500, P=0.013；U=7.000, P＝0.050；U=6.000, P=0.022；U=6.000, P=0.022；U=7.000, P＝0.050；），其余菌属的差异均无统计学意义（均P>0.05）（见图7C）。
在种水平上，高脂组PD 0.5仔鼠肠道Bacteroides_SP._SLC1-38的丰度显著高于对照组（U=3.000, P=0.007），其余菌种的差异均无统计学意义（均P>0.05）（见图7C）。
LEfSe分析统计了对各组间差异的影响大于设定值（LDA Score=3）的差异物种。在属水平上，高脂组PD 0.5仔鼠肠道埃希氏菌属/志贺氏菌属、瘤胃球属、考拉杆菌属、Lachnospiracea_incertae_sedis的丰度较高；在种水平上，高脂组PD 0.5仔鼠肠道Bacteroides_SP. _SLC1-38的丰度较高（见图7D）。
3　讨论
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本研究发现，孕前和孕期高脂饲料喂养对PD 0.5仔鼠的体重、肠道质量、肠道系数以及肠道绒毛和隐窝表面单层柱状细胞形态无显著影响；但可导致PD 0.5仔鼠肠道瘤胃球菌属、考拉杆菌属、Lachnospiracea_incertae_sedis、韦荣氏球菌属、黄杆菌属、埃希氏菌属/志贺氏菌属和Bacteroides_sp._SLC1-38的丰度显著增加，同时结肠组织Claudin-1，Lysozyme和Reg3γ和Alpha-defensin 5基因的表达水平增加。
Myles等人发现与标准低脂饲料（脂肪供能比10%）组相比，孕期高脂饲料（脂肪供能比40%）喂养的小鼠，断乳子代的肠道菌群α多样性（Shannon指数）降低[12]。Chu等人建立前瞻性队列，通过膳食问卷评估母亲分娩前近一个月的膳食脂肪摄入量，并收集新生儿胎粪，进行16S rRNA测序和分析，结果发现母亲高脂饮食组（膳食脂肪摄入量43.1%）的新生儿胎粪微生物β多样性与对照组（膳食脂肪摄入量24.4%）间存在显著差异[17]。本研究以大鼠为模型，于孕前8周开始高脂饲料喂养并持续至分娩，高脂组PD 0.5仔鼠肠道菌群的α多样性有增加的趋势，但无统计学差异。这些研究结果提示，新生儿肠道菌群多样性可能受母亲孕期膳食组分的影响，但未来仍需要有更多的实验室研究和临床试验提供高质量的证据。
瘤胃球菌属在宿主碳水化合物的代谢中起着至关重要的作用。Ma等人发现孕期和哺乳期高脂饲料喂养的日本猕猴，其1岁子代的肠道瘤胃球菌属的丰度增加[11]。研究发现成年糖尿病患者肠道瘤胃球菌属的丰度增加[18]。另一项研究通过比较肥胖和非肥胖人群的粪便菌群，发现肥胖组酒神瘤胃球菌、卵瘤胃球菌丰度显著增加[19]。研究发现高脂饮食更有可能导致大量产生丙酸和乙酸的细菌在肠道聚集，如韦荣氏球菌科和考拉杆菌属，两者的丰度与体重增加等肥胖相关的代谢参数成正相关[20-21]。Lachnospiracea_incertae_sedis参与碳水化合物的代谢，可以产生短链脂肪酸[22-23]。母亲高脂饮食增加子代超重肥胖、二型糖尿病、心血管疾病等代谢性疾病等的发生风险[24]。本研究发现高脂组PD 0.5仔鼠肠道的瘤胃球菌属、考拉杆菌属、韦荣氏球菌属和Lachnospiracea_incertae_sedis的丰度显著增加，其是否能持续到幼年甚至成年，并参与肥胖和二型糖尿病等的发生，尚需进一步研究。
黄杆菌属是一种条件致病菌，其丰度增加与潜在感染风险增加相关。埃希氏菌属/志贺氏菌属可以黏附和侵入肠道上皮细胞，释放毒素和代谢产物，其丰度的增加可能与肠道黏膜的损伤和炎症反应有关[25-26]。Occludin，ZO-1，Claudin-1等蛋白参与紧密连接的形成，在肠道上皮细胞构成的物理屏障中发挥重要的防护作用[27]。MUC2是杯状细胞合成和分泌的黏蛋白，作为肠道黏液的重要成分，参与形成肠道物理屏障[28]。抗菌肽参与组成了肠道黏膜的化学屏障：Alpha-defensin 5和Lysozyme可抑制革兰阳性菌和革兰阴性菌，Reg3γ可以抑制革兰阳性菌[29-30]。我们检测了这些蛋白的基因表达水平，表征肠道的物理屏障和化学屏障功能，评估其抵御微生物和防止致病菌感染的水平。本研究发现高脂组PD 0.5仔鼠结肠中Claudin-1，Lysozyme，Reg3γ和Alpha-defensin 5等的mRNA表达水平显著高于对照组。这些基因表达水平的增加可能是一种内源性保护肠上皮屏障的补偿机制，通过增加肠道上皮细胞的紧密连接和抗菌肽的分泌，保护宿主免受黄杆菌属、埃希氏菌属/志贺氏菌属等致病细菌感染。
本研究对孕前和孕期高脂饲料喂养的新生大鼠的肠道病理形态、屏障功能以及菌群多样性、组成和丰度进行了综合分析，加深了对新生大鼠肠道菌群的理解, 探究了孕前和孕期高脂喂养对新生大鼠肠道菌群的影响，结果提示孕前和孕期的高脂饲料喂养，可能导致新生大鼠肠道代谢相关菌和致病菌的丰度增加。本研究存在一定局限性，仅对新生大鼠的肠道菌群进行16s rRNA分析，未开展宏基因组测序，后续需要展开深入研究。综上所述，本研究发现孕前和孕期高脂饲料喂养会改变新生大鼠肠道菌群的组成。
基金
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  • 北京市教育委员会科技/社科计划项目(KZ202210025039)
文献
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参考文献 引证文献
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doi: 10.20043/j.cnki.MPM.202311248
  • 接收时间：2023-11-13
  • 首发时间：2026-03-19
  • 出版时间：2024-02-25
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  • 收稿日期：2023-11-13
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北京市教育委员会科技/社科计划项目(KZ202210025039)
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    首都医科大学公共卫生学院营养与食品卫生学系，北京 100069

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余焕玲，E-mail：
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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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