摘要
蜜蜂(Apis mellifera)是全球范围内至关重要的授粉昆虫，同时也是研究发育与行为模式的重要生物模型，兼具显著的经济、生态及科研价值。蜜蜂肠道微生物，作为其生存的“共生体”，借助社会行为互动传播，对蜜蜂的发育与健康发挥着关键作用。这些微生物不仅助力蜜蜂消化吸收营养物质，还能有效抵御病原体侵袭，增强宿主免疫力。近年来，蜜蜂已成为肠道微生物研究的热门模型。科研人员不仅深入分析了蜜蜂肠道微生物群的组成与功能，还积极探索了菌株的多样性与特定功能。本文综述了蜜蜂肠道微生物群的时空动态变化特性、影响微生物群落结构的因素、微生物群对蜜蜂生物学特性及健康的影响，以及微生物的功能性应用，旨在为蜜蜂肠道微生物的研究与实践应用提供有价值的参考。
蜜蜂(Apis mellifera)作为一种不可或缺的传粉昆虫，在推动全球农业的可持续发展和维护生态系统的整体健康中扮演着至关重要的角色。然而，近年来的统计显示，全球蜜蜂种群正遭受寄生虫侵袭、化学杀虫剂污染及营养不良等多重挑战，导致种群数量大幅下
1 蜜蜂肠道菌群组成与时空特征
1.1 蜜蜂肠道微生物的组成
肠道作为肠道微生物栖息和繁衍的核心区域，其微环境对微生物的组成、结构和功能具有显著影响，其中，不同性别和级型的蜜蜂，其肠道微生物组成存在明显区别(
| Phylum | Phylotype | Species | Primary gut location |
|---|---|---|---|
| Core bacteria | |||
| Proteobacteria | Gilliamella (Gamma-1) | Gilliamella apicola | Adult ileum lumen and queen guts |
| Gilliamella apis | Adult pylorus | ||
| Proteobacteria | Snodgrassella (Beta) | Snodgrassella alvi | Adult ileum wall |
| Firmicutes |
Lactobacillus (Lactobacillus Firm-5) |
Lactobacillus apis Lactobacillus helsinborgensis Lactobacillus huangpiensis Lactobacillus juensis Lactobacillus kimbladii Lactobacillus kullabergensis Lactobacillus laiwuensis Lactobacillus melliventris Lactobacillus rizhaonensis | Adult ileum and rectum, queen, and drone guts |
| Firmicutes |
Bombilactobacillus (Lactobacillus Firm-4) |
Bombilactobacillus mellifer Bombilactobacillus mellis | Adult rectum, queen, and drone guts |
| Actinobacteria | Bifidobacterium |
Bifidobacterium apousia Bifidobacterium asteroides Bifidobacterium choladohabitans Bifidobacterium coryneforme Bifidobacterium indicum Bifidobacterium mellis Bifidobacterium mizhiense Bifidobacterium polysaccharolyticum | Adult rectum |
| Non-core gut-restricted bacteria | |||
| Proteobacteria | Frischella (Gamma-2) | Frischella perrara | Adult pylorus and ileum |
| Proteobacteria | Bartonella (Alpha-1) |
Bartonella apis Bartonella apihabitans Bartonella choladocola | Adult hindgut |
| Proteobacteria | Commensalibacter (Alpha-2.1) | Commensalibacter sp. | Adult hindgut and queen guts |
| Bacteroidetes | Apibacter | Apibacter adventoris | Adult hindgut |
| Environmental bacteria | |||
| Proteobacteria | Bombella (Alpha-2.2) |
Bombella apis Parasaccharibacter apium Saccharibacter sp. | Adult crop, larval and queen guts, and hive |
| Firmicutes | Apilactobacillus |
Apilactobacillus apinorum Lactobacillus apinorum Apilactobacillus kunkeei Apilactobacillus nanyangensis Apilactobacillus xinyiensis Apilactobacillus zhangqiuensis | Adult crop, larval gut, nectar, honey, hive for Apil. kunkeei, and adult gut for other species |
| Firmicutes | Fructobacillus |
Fructobacillus apis Fructobacillus fructosus | Adult gut for Fru. apis, larval and adult guts, and hive for Fru. fructosus |
| Pathogens | |||
| Proteobacteria | Hafnia | Hafnia alvei | Adult gut |
| Proteobacteria | Serratia | Serratia marcescens | Adult gut |
1.2 蜜蜂肠道微生物的时空特征
1.2.1 蜜蜂肠道微生物的时间分布特性
蜜蜂肠道微生物群落的结构与多样性深受其个体发育阶段、年龄增长及社会分工的复杂影响。作为完全变态发育的昆虫，蜜蜂的个体发育过程需经历卵、幼虫、蛹和成虫4个阶
蜂王在其生命周期的不同阶段，肠道内的优势菌群也发生显著变化。幼虫期及新出房时的蜂王，肠道优势菌为埃希氏菌属(Escherichia)、吉列姆氏菌属(Gilliamella)，而随蜂龄增长和生理状态变化，成熟蜂王的肠道内则主要由共生杆菌属(Commensalibacter)、大黄蜂菌属(Bombella)、乳杆菌属Lactobacillus) Firm-4和Lactobacillus Firm-5等菌种占据主导地位，这一变化归因于蜂王自身的生理发育、饮食变化以及与工蜂间复杂的互动关
此外，蜂群内部的劳动分工也对蜜蜂的肠道微生物群落产生深远影
1.2.2 蜜蜂肠道中微生物的空间分布特性
蜜蜂肠道细菌的分布在其复杂的消化系统中展现出鲜明的空间特异性，这一现象不仅揭示了微生物与宿主间的紧密互作关系，也体现了它们在肠道内独特的生态位(
图1 蜜蜂肠道微生物的空间位置分布(改自文献[
Figure 1 Spatial location distribution of honeybee gut microbes (adapted from literature [8]).
蜜囊是蜜蜂体内用于暂时储存花蜜的器官，其内部细菌丰度相对较低，主要栖息着一些随花蜜进入或通过接触蜂箱等蜂具而引入的微生物，如Apilactobacillus和Bombella，它们与花蜜的初步处理过程相伴而
相比之下，蜜蜂的后肠成为了细菌聚集的主要场所。这一区域由稳定的角质层保护肠壁，确保了内部环境的相对稳定，同时，那些未能在中肠被完全消化的膳食化合物在此累积，为栖息于此的微生物群提供了丰富的碳源与氮源，进一步促进了这些微生物的生长与繁
2 影响蜜蜂肠道微生物群的因素
蜜蜂为全球农业带来了显著的生态与经济效益。然而，蜜蜂的生存面临着遗传、营养、农药暴露和病原体侵袭等多重威胁，这些因素不仅严重影响蜜蜂的健康状况，同时也深刻改变着蜜蜂肠道微生物群落的构成和丰度。
2.1 宿主遗传的调控
蜜蜂的遗传多样性是塑造其肠道微生物群多样性的关键因素之
2.2 食物和营养的双重驱动
在蜂群中，花蜜作为碳水化合物的来源，与富含多样化营养成分如碳水化合物、氨基酸、脂类及维生素的花粉相辅相成，共同为蜂群提供必需的营养物
花粉在维持蜜蜂健康肠道菌群生态平衡中发挥着重要作用，其质量和新鲜度在塑造蜜蜂肠道微生物群中起着至关重要的作用。摄入低营养价值的桉树花粉不仅减少了Lactobacillus Firm-4、Bifidobacterium spp.等有益菌的数量，还促进了非核心菌如蜜蜂巴尔通氏体(Bartonella apis) DSM 29779的滋生，进而削弱蜜蜂的免疫系统，这为致病菌、微孢子虫等病原体的入侵提供了可乘之
当蜜源植物稀缺时，养蜂人常通过补充糖源来保障蜜蜂的能量需求，然而这一举措也会微妙地影响蜜蜂肠道菌群的结构。例如，夏季短期饲喂蔗糖能改变消化道内根瘤菌科(Rhizobiaceae)、醋杆菌科(Acetobacteraceae)、昆基氏蜜蜂乳杆菌(Apilactobacillus kunkeei) ATCC 700308和稀罕弗里希氏菌(Frischella perrara) ATCC BAA-2450的相对丰
2.3 病原体的侵袭
病原体的侵袭显著扰乱了蜜蜂肠道内微妙的微生物生态平衡。与健康蜜蜂幼虫相比，感染欧洲幼虫腐臭病(European foulbrood, EFB)和蜜蜂囊状幼虫病病毒(sacbrood virus, SBV)的蜜蜂幼虫肠道微生物数量会显著降
2.4 农药化学品的挑战
蜜蜂健康状况的下滑与杀虫剂和抗生素的过度使用、环境污染密切相
Hotchkiss
四环素作为养蜂业中的常用抗生素，其使用虽旨在防治疾病，但却悄然削弱了蜜蜂的肠道健
除农药与抗生素外，纳米塑料(nano-plastics, NPs)、微塑料(micro-plastics, MPs)及重金属等环境污染物也被发现能够破坏蜜蜂的肠道微生物群。100 nm聚苯乙烯颗粒(polystyrene particles, PS)处理降低了肠道中Lactobacillus和Bifidobacterium的相对丰度，使得蜜蜂更易感染致病菌蜂房哈夫尼菌(Hafnia alvei) ATCC 13337，从而增加死亡
3 蜜蜂肠道微生物群的功能
蜜蜂肠道微生物群已成为肠道微生物学领域内一个极具吸引力和前瞻性的研究模
图2 肠道微生物在蜜蜂健康中的作用概述图
Figure 2 Overview of roles of the gut microbiome in honey bee health.
3.1 肠道微生物对病原体防护的影响
Raymann
抗生素的滥用则对蜜蜂肠道微生物群造成了严重破坏，导致微孢子虫数量激
3.2 肠道微生物对蜜蜂发育和行为的影响
蜜蜂肠道内的微生物群落对蜜蜂的生长发育和学习记忆行为具有重要的作用。具体而言，一个健全完整的微生物群落与卵黄素及胰岛素信号通路基因表达的上调、嗅觉功能的增强、行为模式的转变、神经系统的成熟与突触传递效率的提升，以及肠道、血淋巴和脑组织中氨基酸、甘油磷脂、激素和短链脂肪酸含量的增加有
肠道菌群对蜜蜂行为的影响同样不容忽视。通过伸吻反应试验，科研人员观察到肠道微生物群在调节蜜蜂对蔗糖的敏感性以及嗅觉学习记忆能力方面发挥着重要作用，拥有丰富且多样菌株的肠道微生物群促进了蜜蜂正常的味觉行为反应，使其对低浓度蔗糖更为敏
3.3 肠道微生物对蜜蜂营养代谢的影响
蜜蜂依赖富含糖分的花蜜以及富含氨基酸、脂质和维生素的花粉作为其主要食物来
4 蜜蜂益生菌的潜力
近年来，抗生素在动物养殖中的广泛应用引发了多重问题，包括抗药性的出现、动物产品中抗生素残留超标以及环境污染加剧，这些问题在一定程度上阻碍了产业的发展并降低了动物产品的质量。鉴于益生菌的稳定性、无致病性、易于扩增及适应肠道微生态等特性，其作为抗生素的替代方案在饲料添加剂领域展现出了广阔的应用潜力。在养蜂业中，益生菌的应用已不仅限于预防和治疗蜂巢内的微生物感染，更成为维护蜜蜂健康的重要手段。然而，当前市面上多数蜜蜂益生菌产品并非源自蜜蜂自身的原生微生物群落，而是来自食品工业的细菌和真菌。尽管这些外来菌种在一定程度上能够保护蜜蜂健康，但它们往往难以在蜜蜂体内稳定定
针对蜜蜂美洲幼虫臭病等特定疾病，益生菌的应用研究也取得了积极进展，Daisley
尽管一些结果很有希望，但在蜜蜂中使用益生菌的潜力仍不清楚，尤其是在田间条件下。然而，益生菌及其相关技术的研究与应用正逐步改变着养蜂业的面貌，为蜜蜂健康与产业可持续发展注入了新的活力。
5 蜜蜂肠道微生物的功能研究技术手段
在研究蜜蜂肠道共生菌与宿主之间的相互作用时，科学家们发现蜜蜂与人类的肠道存在诸多相似之处，这一发现使得蜜蜂成为研究肠道微生物的重要模式生物，对于医学、农业以及生态学等多个领域都具有深远的意
蜜蜂在抵抗病毒侵袭时，主要依赖于自身的免疫反应，其中RNAi是昆虫(包括蜜蜂在内)的一种至关重要的抗病毒防御机制。通过运用CRISPR-Cas9这一先进的基因编辑技术，能够精准地编辑蜜蜂肠道内的共生菌，从而实现靶向性地对抗病原物的目的，蜜蜂肠道核心菌群参与抵御寄生疾病，对原生肠道共生体的基因工程改造为蜜蜂疾病防控开辟了新途
除了使用基因工程改造肠道菌群外，还能通过一些其他的科研技术研究肠道菌群的潜在价值。例如，通过微流控单细胞液滴培养蜜蜂肠道菌，能够研究蜜蜂肠道微生物群的多样性以及蜜蜂肠道共生菌存在的宿主特异性适应机制，这有助于寻找一些难以捉摸的细
6 展望
近年来，随着公众对蜜蜂健康问题的日益关注，蜜蜂肠道微生物的研究与应用也迎来了前所未有的增长。截至目前，研究表明蜜蜂肠道微生物群对宿主的消化、解毒、行为、病原体防御和免疫系统都具有实质性影响。被剥夺正常微生物群的蜜蜂和微生物群被化学物质破坏的蜜蜂表现出一系列健康缺陷，包括摄食行为的变化、对病原体的更易感性，以及蜂群整体的高死亡率。相比之下，对无菌蜜蜂进行单菌或混菌定殖可以帮助其微生物群恢复部分功
尽管大量证据表明肠道共生体对蜜蜂有好处，但这些影响背后的分子机制在很大程度上是未知的。例如，肠道微生物群的特定成员已被证明可以防止病原体增殖并保护宿主免受病原体诱导的死亡，但尚不清楚保护是来自宿主免疫反应和/或微生物之间的直接相互作
最近的另一个研究方向涉及脑-肠轴。长期以来，蜜蜂一直被用作研究行为的模型，从认知到社会互动，行为分析已经非常成熟。最近的研究利用这些行为分析和无菌蜜蜂来探索微生物群在味觉、嗅觉学习和蜂群社交网络中的作用，并研究它们在蜜蜂身体不同区域发挥的转录和代谢功能，结果表明，原生微生物群的共同作用塑造了蜜蜂的行
蜜蜂的肠道稳态与其健康状态之间存在着微妙的平衡，一旦这一平衡被打破，病原体便可能乘虚而入，对蜜蜂健康构成严重威胁。在面对环境压力源时，蜜蜂的肠道微生物群往往首当其冲，受到显著影响。遗憾的是，当前多数研究仍局限于分析肠道微生物群的相对丰度或采用定量PCR等方法测定其绝对丰
此外，随着研究的深入，科学家们的视野已不再局限于蜜蜂本身，而是拓展至大黄蜂及其他野生蜜蜂的肠道微生物群，这一转变不仅有助于更全面地保护多样的传粉媒介，还极大地丰富了对于宿主-细菌相互作用及其进化历程的认识。因此，深入研究蜜蜂肠道微生物群的动态变化，不仅对于促进蜜蜂健康具有直接而重要的实际意义，更有助于透过蜜蜂这一独特视角，洞察社会性动物间复杂的跨物种相互作用机制。通过揭示蜜蜂与其肠道细菌之间错综复杂的关系与进化历程，能够为保护这些生态系统中不可或缺的传粉者提供更为坚实的科学支撑。
作者贡献声明
刘建辉：论文构思和设计、资料检索、论文撰写和修订；陈敬：论文资料检索与修订；胡越洋：论文审阅与修订；吴小波：论文构思和设计、论文审阅与修订。
利益冲突
作者声明不存在任何可能会影响本文所报告工作的已知经济利益或个人关系。
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