奶牛耐寒怕热的生理特点,导致其生理机能以及生产性能容易受到外界环境温湿度的影响[1],奶牛处于热应激状态时,采食量下降,激素分泌、瘤胃发酵等生理生化指标受到影响,使得其产奶量下降、免疫机能降低、乳品质量下降[2-3]。反刍动物的瘤胃微生物通过对饲粮纤维和碳水化合物等物质降解发酵,合成微生物蛋白,为反刍动物提供营养物质[4]。奶牛日常能量需求的70%依赖于瘤胃微生物产生的发酵副产物(例如短链脂肪酸),日常蛋白质需求的50%来源于微生物本身[5],因此瘤胃微生物与奶牛营养物质消化吸收、饲料转化率、产奶性能以及机体健康密切相关[6-8]。热应激会改变瘤胃微生物的多样性和丰度[9-10],使淀粉分解菌和纤维降解菌的丰度降低,而且入侵的致病菌与常驻菌形成营养竞争的关系,容易导致胃肠道疾病[11]。瘤胃正常组织形态和内环境稳态是保证瘤胃微生物发挥正常功能的前提条件,热应激可能通过瘤胃上皮黏膜损伤、瘤胃温度及瘤胃液pH的变化等[12-13]影响微生物的定植和繁殖能力,使得物质代谢和能量流动产生障碍,这是导致奶牛生产性能降低的重要原因。本文将总结热应激对瘤胃微生物多样性影响的相关研究结果,从瘤胃组织形态、瘤胃温度及瘤胃液pH等方面探讨热应激影响瘤胃微生物的机制,并解析瘤胃微生物区系与奶牛饲料转化率、产奶量及乳成分之间的关系,旨为生产实践提供一定的理论参考。
1 热应激对瘤胃微生物的影响反刍动物对饲粮的消化依赖于瘤胃内复杂的微生物区系,瘤胃内不同类型的共生厌氧微生物,包括古菌、细菌、真菌、原虫、噬菌体等[14],不同微生物类群可分泌不同的降解酶,对维持奶牛消化和代谢功能至关重要。
环境温湿度是影响奶牛生理健康和生产性能的重要因素之一,目前通常用温湿指数(temperature-humidity index,THI)评价奶牛的热应激程度[15]。轻度热应激时奶牛可通过自身调节抵御影响,当热应激程度加深,超出自身调控限度时,机体热调节能力下降,从而破坏宿主和瘤胃菌群动态的微生态平衡。Tajima等[9]研究发现,将牛舍温度从20 ℃升至33 ℃(环境相对湿度保持60%不变),奶牛瘤胃中产琥珀酸丝状杆菌(Fibrobacter succinogenes)、黄化瘤胃球菌(Ruminococcus flavefaciens)的数量下降,普雷沃氏菌(Prevotella ruminicola)的数量上升。Uyeno等[10]设置与Tajima等[9]相同的环境条件,利用相对先进的RNA-based微生物测序技术发现,环境温度从20 ℃升至33 ℃(相对湿度均为60%)后菌群的结构及多样性均发生了很大变化,其中链球菌(Streptococcus)的丰度增加10倍,纤维分解菌(Fibrobacter)的丰度降低80%,颤螺旋菌属(Oscillospira)的丰度也显著降低,颤螺旋菌属被认为是与肠道屏障完整性及渗透性密切相关的菌属[16]。杜瑞平等[17]报道,当THI处于80.92~88.53时,泌乳中期奶牛产生热应激,瘤胃液总细菌数量极显著降低,纤维分解菌如产琥珀拟杆菌、白色瘤胃球菌及黄化瘤胃球菌的数量显著降低,这3种菌属可分泌大量的纤维素酶和半纤维素酶,是瘤胃中主要的纤维降解菌。另有研究表明,夏季高温高湿环境下,泌乳奶牛粪便中梭菌孢子的数量增多[11],作为条件性致病菌,梭菌属可增加胃肠道上皮屏障及血管通透性,从而诱导炎症反应[18]。由此可见,高温高湿环境可能不利于纤维的降解,奶牛偏好利用淀粉等易消化碳水化合物来减少机体产热,而致病菌的定植增加表明胃肠道的免疫功能可能受到热应激的影响。
2 热应激对瘤胃微生物影响的可能原因 2.1 瘤胃组织形态热应激可能通过影响瘤胃组织形态改变微生物区系。瘤胃组织形态学发育指标包括瘤胃上皮、瘤胃乳头形态和瘤胃壁厚度等。其中瘤胃上皮是吸收关键营养物质如短链脂肪酸、以及Na+和Mg2+等电解质的主要部位[19],还具有调节pH和屏障免疫功能。瘤胃上皮形态遭到破坏时,会影响黏附在瘤胃壁上的菌群的生理活性[20]。热应激可通过破坏瘤胃黏膜上皮细胞紧密连接,使瘤胃黏膜绒毛萎缩脱落,增加瘤胃黏膜屏障通透性[21]。屏障通透性增高致使细菌及其代谢产物移位,导致瘤胃内菌群结构发生变化。瘤胃乳头形态关系到瘤胃表皮与饲粮的接触面积,从而影响营养物质的消化吸收效率。瘤胃乳头的发育主要靠发酵碳水化合物产生的挥发性脂肪酸(volatile fatty acids,VFA)的刺激[22],高温高湿环境下,奶牛采食量减少,进入瘤胃的发酵底物减少,从而导致瘤胃乳头宽度、周长以及表面积减少[23]。Yazdi等[24]发现,与舒适环境(20.7 ℃,THI=65.2)相比,热应激状态(29.9~41.0 ℃,THI≥85.0)的荷斯坦犊牛瘤胃乳头高度增加了51%,乳头顶部宽度降低了40%,饲料利用效率降低,不利于瘤胃发酵和内环境的稳定。
2.2 瘤胃温度热应激可能通过升高瘤胃温度改变微生物区系。瘤胃温度通常比直肠温度高1~2 ℃,当其稳定在38~42 ℃时可维持瘤胃微生物区系生存的正常环境[25]。环境压力因素会影响奶牛的体温调节能力。Scharf等[12]对比环境控制舱和自然环境热应激下的奶牛体温调节反应相似度发现,环境温度每上升1 ℃,2种试验条件下的奶牛瘤胃温度分别随之上升0.04和0.03 ℃。而当瘤胃温度超过40 ℃时,原虫的生存能力下降,细菌占据竞争优势,大量淀粉被细菌发酵成丁酸,然后转变成乳酸,而瘤胃壁对乳酸的吸收速度较慢,使瘤胃pH下降[26],从而影响其他微生物的生存环境。
2.3 瘤胃液pH和渗透压热应激可能通过降低瘤胃液pH和渗透压改变微生物区系。瘤胃液正常pH在6.2~6.8之间,高于或低于正常范围都会改变菌群结构[27]。研究表明,当环境温度及相对湿度分别从23.6 ℃、50.3%上升至33.2 ℃、63.0%时,热应激会使得瘤胃液乳酸含量增加,pH呈现降低趋势[13],当THI达到82时,瘤胃内容物的pH和渗透压均显著降低[28]。热应激状态下,THI每上升1个单位,奶牛饮水量增加0.96~1.80 L[29],导致瘤胃液被稀释,而且流经瘤胃上皮的血液量减少,酸碱平衡被打破,唾液分泌量以及其中的碳酸氢根离子(HCO3-)含量减少,从而引起瘤胃内环境尤其是pH和渗透压的改变[30]。在极低pH下,牛链球菌占据竞争优势,从而影响其他微生物定植[31],而且瘤胃液pH较低不利于纤维分解菌的生长,进而限制纤维的消化和蛋白质的合成,还会诱导生长期或细胞裂解期间的革兰氏阴性菌外膜释放更多脂多糖,容易引起胃肠道炎症反应[32]。
3 瘤胃微生物区系组成的变化对奶牛生产性能的影响热应激条件下,高温高湿环境导致奶牛采食量减少,消化道蠕动缓慢,瘤胃发酵功能及上皮结构被破坏,用于乳汁合成的营养物质来源减少,同时机体激素分泌机能紊乱,乳腺发育和排乳反应受到抑制,最终影响奶牛生产性能[33]。瘤胃微生物对瘤胃发酵、饲料纤维降解及微生物蛋白合成至关重要,热应激条件下,奶牛饲料转化率、产奶量和乳成分等生产性能受到影响而发生改变,这种改变可能与瘤胃微生物种类及丰度的变化具有潜在联系。
3.1 饲料转化率热应激对瘤胃微生物的影响可能改变饲料转化率。Hill等[34]对328头荷斯坦奶牛进行为期8年的研究后发现,在THI为49~59的相对舒适环境内,饲料转化率随着THI的升高而升高[35],但是当日均THI从53.0升至76.5时, 奶牛饲料转化率显著下降(1.66 vs. 1.56),反刍动物瘤胃微生物对饲料降解及物质代谢起关键作用,使得其与饲料转化率具有直接联系。热应激条件下,瘤胃微生物降解能力下降和功能分解菌数量减少,不利于营养物质消化吸收,这是导致饲料转化率降低的重要原因[36]。奶牛瘤胃中存在与饲料转化率相关的特定微生物,并且相关性较高的菌群分别占瘤胃液和固体内容物菌群的21.7%和29.6%[35]。瘤胃微生物发酵产生的短链脂肪酸是反刍动物的主要能量来源,饲料转化率高和低的奶牛消化产生的短链脂肪酸总含量相差可达10%,并且丙酸、丁酸、戊酸和异戊酸在饲料转化率高的奶牛瘤胃液中含量更高[37],热应激导致的瘤胃微生物区系失衡可能会改变瘤胃发酵模式,从而影响饲料转化率。Weimer等[38]分析了瘤胃菌群改变对饲料转化率的影响,利用瘤胃插管将不同饲料转化率奶牛瘤胃中约95%的内容物相互转移,发现瘤胃菌群的改变会不同程度地影响奶牛原来的饲料转化率。研究表明,奶牛饲料转化率的增强伴随着毛螺菌科(Lachnospiraceae)、拟杆菌门(Bacteroidetes)及其包括的菌属丰度的升高[39],毛螺菌科的增加可促进碳水化合物的降解及丁酸的产生[40],拟杆菌门与厚壁菌门(Firmicutes)比值的增加可减少脂肪沉积[8],从而加快物质循环和能量流动,以满足奶牛的泌乳需求。拟杆菌属(Bacteroidetes)、普沃氏菌属(Prevotella)以及纤维降解菌[包括溶糊精琥珀酸弧菌(Succinivibrio dextrinosolvens)、埃氏巨型球菌(Megaspheara elsdenii)和产琥珀酸丝状杆菌]在高饲料转化率奶牛瘤胃菌群中表现出较高的丰度[38, 41]。拟杆菌属和普沃氏菌属降解饲料中的碳水化合物和蛋白质,参与蛋白质的从头合成,并以其他纤维降解菌的降解产物作为能量来源[42];另外3种纤维降解菌的主要发酵产物是琥珀酸(丙酸的前体)以及乙酸,并能以乳酸为前体合成丁酸,容易被瘤胃壁吸收用于肝脏糖异生,从而提高饲料转化率和产奶性能[37]。甲烷短杆菌属(Methanobrevibacter)和链球菌(Streptococcus bovis)在高饲料转化率的奶牛中丰度较低[41]。在热应激导致采食量降低的情况下,机体偏向于利用碳水化合物等热增耗较小的营养物质,产甲烷菌代谢底物氢气(H2)和二氧化碳(CO2)来源减少[43],使得其在瘤胃内的繁殖能力减弱,以此减少甲烷的产生和能量损失,同时热应激条件下,瘤胃内环境变化导致瘤胃链球菌的丰度显著增加,纤维分解菌的丰度大幅降低,链球菌的大量增殖容易造成乳酸的大量积累[41],不利于纤维物质的降解,从而改变瘤胃发酵参数和饲料转化率。
3.2 产奶量及乳成分热应激对瘤胃微生物的影响可能改变产奶量及乳成分。Indugu等[7]采用减少采食量作为对照组的方法,发现相较于舒适环境(20 ℃,相对湿度为55%),热应激(32~36 ℃,相对湿度为40%)使产奶量、乳蛋白产量、乳蛋白率、4%乳脂校正乳和乳脂产量分别降低17%、4%、19%、23%和19%。微生物在瘤胃内充分繁殖时,分泌各种消化酶,这些消化酶能将大量不能被奶牛直接利用的物质转化成能被奶牛利用的高质量的营养素,包括VFA和微生物蛋白等,作为泌乳的物质基础[44]。热应激引起的乳成分改变可能与瘤胃微生物组成和多样性的改变有关。普雷沃氏菌、S24-7和琥珀弧菌科(Succinivibrionaceae)在高产奶量奶牛瘤胃中丰度更高,普雷沃氏菌属和普雷沃氏菌科都属于拟杆菌门,这些菌群都与乳脂率和乳蛋白率呈负相关[7],这与Jami等[8]的研究一致。Jami等[8]还发现厚壁菌门和拟杆菌门的比例与乳脂率呈极显著正相关。瘤胃微生物与乳脂组成也密切相关。例如,丁酸弧菌属(Butyrivibrio)、Bulleidia、柯林斯菌科与共轭亚油酸反式-10,顺式-12和反式-10异构体的生成密切相关,其中丁酸弧菌具有分解半纤维素、水解蛋白质和分解尿酸的活性[45]。
4 小结综上所述,热应激可能通过降低采食量改变瘤胃乳头形态,破坏瘤胃上皮黏膜完整性并增加其通透性,使瘤胃温度升高,降低瘤胃液pH及渗透压来改变瘤胃微生物的多样性,进而影响奶牛的饲料转化率、产奶量及乳成分等生产性能。由于瘤胃菌群生态系统的复杂性和测序技术的限制,目前关于热应激对奶牛瘤胃微生物影响的报道中,覆盖的菌群种类较少,并且缺乏具体的丰度数据,未来的研究应利用更先进的测序技术,全面解析热应激条件下瘤胃微生物多样性的变化,尤其是与营养物质消化代谢密切相关的功能降解菌, 并同时与生产性能做关联性分析,从整体上深入阐明热应激条件下瘤胃微生物的改变对奶牛生产性能的调控机理。
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