Insect endosymbiont proliferation is limited by lipid availability.
Insect endosymbiont proliferation is limited by lipid availability.
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DOI：
10.7554/elife.02964
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发表时间：
2014-07-15
期刊：
影响因子：
7.7
通讯作者：
Lemaitre B
中科院分区：
文献类型：
--
作者：
Herren JK;Paredes JC;Schüpfer F;Arafah K;Bulet P;Lemaitre B
波氏螺原体是一种母体传播的细菌内共生体，与黑腹果蝇自然相关。波氏沙门氏菌居住在细胞外的血淋巴中，在那里它必须获得代谢物来维持增殖。在这项研究中，我们发现螺旋体增殖特异性地消耗宿主血淋巴二酰基甘油酯，这是由脂蛋白Lpp运输的主要脂类。rnai介导的Lpp表达下调，可减少循环脂质量，抑制螺旋体增殖，表明细菌增殖需要血脂。总之，我们的研究表明，昆虫内共生体从宿主血淋巴中的转运脂蛋白中获得特定的脂质代谢物。此外，我们表明，这种内共生体的增殖是有限的可用的血脂。由于脂质利用率受营养状况的强烈影响，这一特性可以限制宿主营养限制条件下内共生菌的过度增殖。DOI: http://dx.doi.org/10.7554/eLife.02964.001所有动物体内都有大量无害微生物。通常，参与这些互动的两个伙伴将相互依赖以茁壮成长：微生物支持重要的宿主功能，作为回报，宿主提供了一个安全的生活场所和持续的食物供应。许多与动物密切相关的微生物已经失去了从宿主以外的来源获取营养的能力，无法靠自己生存。然而，在许多情况下，提供给微生物的营养来源和类型是未知的。在昆虫中发现的最常见的微生物物种之一是螺旋体。这种微生物大量生活在充满昆虫体腔的液体中，称为血淋巴。这些微生物从母亲传给后代，在某些情况下可以给昆虫带来好处；例如，被螺旋体感染的苍蝇似乎可以免受某些寄生虫的感染。不幸的是，由于很难研究昆虫与微生物的关系，人们对这两个物种之间的生理相互作用知之甚少。Herren等人研究了螺旋体与黑腹果蝇之间的关系。在正常情况下，螺原体只会缩短被感染蝇的寿命。这说明螺原体对寄主的总体健康影响不大，仅对老蝇的生存和产卵能力产生负向影响。当果蝇获取营养物质的途径有限时，它们携带的螺旋体数量会减少，但果蝇不会失去健康。这表明螺原体的生长依赖于果蝇饮食中的某些东西。为了了解哪些营养物质对果蝇螺原体的生长是重要的，Herren等人分析了果蝇的血淋巴，发现当营养物质有限时，被称为脂质的脂肪分子更少。携带螺旋体的健康果蝇的血淋巴中的脂质也较少，这表明这些是螺旋体的食物。事实上，果蝇将脂质运输到血淋巴所需的一种蛋白质失活，减少了这些果蝇体内螺旋体的生长。Herren等人得出结论，螺原体在宿主体内的生长受到血淋巴中脂质可用性的限制。由于这是依赖于饮食，对脂质的依赖使螺旋体的生长与其宿主的营养状况相结合。Herren等人推测，这一机制降低了窝藏微生物的适应度成本，防止了微生物不受控制的增殖所带来的破坏性后果。此外，螺原体对脂质的偏好可以解释为什么它有助于保护苍蝇免受寄生虫感染，因为许多寄生虫也依赖于脂质来生长。Herren等人认为这一策略也可用于其他动物-微生物关联。DOI: http://dx.doi.org/10.7554/eLife.02964.002
Spiroplasma poulsonii is a maternally transmitted bacterial endosymbiont that is naturally associated with Drosophila melanogaster. S. poulsonii resides extracellularly in the hemolymph, where it must acquire metabolites to sustain proliferation. In this study, we find that Spiroplasma proliferation specifically depletes host hemolymph diacylglyceride, the major lipid class transported by the lipoprotein, Lpp. RNAi-mediated knockdown of Lpp expression, which reduces the amount of circulating lipids, inhibits Spiroplasma proliferation demonstrating that bacterial proliferation requires hemolymph-lipids. Altogether, our study shows that an insect endosymbiont acquires specific lipidic metabolites from the transport lipoproteins in the hemolymph of its host. In addition, we show that the proliferation of this endosymbiont is limited by the availability of hemolymph lipids. This feature could limit endosymbiont over-proliferation under conditions of host nutrient limitation as lipid availability is strongly influenced by the nutritional state. DOI: http://dx.doi.org/10.7554/eLife.02964.001 All animals host a large number of harmless microbes. Often the two partners involved in these interactions will depend on each other to thrive: microbes support important host functions and in return the host provides a safe place to live and a continuous supply of food. Many microbes that are intimately associated with animals have lost the ability to gain nutrients from sources other than their host and are unable to survive on their own. However, in many cases, the source and the type of nutrients provided to the microbes are unknown. One of the most common microbial species found in insects is Spiroplasma. This microbe lives in very large numbers in the fluid that fills the body cavities of insects, called the hemolymph. The microbes are transmitted from mother to offspring, and in some circumstances can provide benefits to the insects; for instance, Spiroplasma-infested flies appear to be protected against infection by some parasites. Unfortunately, as it is difficult to study insect–microbe relationships, little else is known about the physiological interactions between these two species. Herren et al. studied the association between Spiroplasma and the fly Drosophila melanogaster. Under normal conditions, Spiroplasma only reduces the life span of the infested fly. This indicates that Spiroplasma has a low impact on the general fitness of its host, only negatively affecting the survival and egg laying ability of old flies. When flies had limited access to nutrients, the number of Spiroplasma they carried was reduced, without the flies losing fitness. This suggests that Spiroplasma growth is dependent on something in the flies' diet. To understand which nutrients are important for the growth of Spiroplasma in Drosophila, Herren et al. analyzed the hemolymph of flies and found that there are fewer fatty-molecules, called lipids, when nutrients are limited. Healthy flies carrying Spiroplasma also have fewer lipids in their hemolymph, suggesting that these are what Spiroplasma feed on. Indeed, inactivating a protein required by the fly to transport lipids to the hemolymph reduced the growth of Spiroplasma in these flies. Herren et al. concluded that the growth of Spiroplasma inside its host is limited by the availability of lipids in the hemolymph. Since this is dependent on diet, the dependence on lipids couples the growth of Spiroplasma to the nutritional state of its host. Herren et al. speculate that this mechanism reduces the fitness cost of harboring the microbes and prevents the damaging consequence of an uncontrolled proliferation of the microbes. Moreover, Spiroplasma's preference for lipids may explain why it helps to protect flies against parasitic infection, as many parasites also rely on lipids for their growth. Herren et al. suggest this strategy could also be used in other animal–microbe associations. DOI: http://dx.doi.org/10.7554/eLife.02964.002