Local Adaptation of Bacterial Symbionts within a Geographic Mosaic of Antibiotic Coevolution
Local Adaptation of Bacterial Symbionts within a Geographic Mosaic of Antibiotic Coevolution
复制标题
DOI：
10.1128/aem.01580-19
复制
发表时间：
2019-12-01
影响因子：
4.4
通讯作者：
Currie, Cameron R.
中科院分区：
文献类型：
--
作者：
Caldera, Eric J.;Chevrette, Marc G.;Currie, Cameron R.
协同进化的地理镶嵌理论认为，协同进化动力超越了局部协同进化，由以下三个部分组成：地理选择镶嵌、协同进化热点和特征重组。目前尚不清楚GMC是否适用于细菌，因为水平基因转移和世界性传播可能违反理论假设。在这里，我们在一种产生抗生素的细菌共生体(伪心霉属)中测试关键的GMC预测，该共生体可以保护种植新热带真菌的蚂蚁(牙科无刺蚁)的作物免受特殊病原体(Ecovopsis)的侵袭。我们发现，与来自哥斯达黎加的群体相比，来自巴拿马的牙假单胞菌群体对常见Ecovopsis病原体的假单胞菌的抑制作用更高。此外，巴罗科罗拉多岛(BCI)上的巴拿马运河带假单胞菌种群是局部适应的，而相邻的两个种群不是本地适应的，这与GMC预测的选择镶嵌和被适应不良区域包围的适应热点一致。适应不良是由不一致的假单胞菌-埃斯科沃普斯种群遗传结构形成的，而在巴拿马运河洪水泛滥后，BCI上的地理隔离促进了局部适应。对29个假单胞菌菌株的抗生素潜力的基因组评估发现，尽管核心基因组中的遗传多样性较低，但BCI菌株中存在多样化和独特的生物合成基因簇。抗生素抑制的强度与单个生物合成基因簇的存在与否或寄生虫的位置无关。相反，生物合成基因簇已经经历了选择性的扫描，这表明赋予抗生素效力长期维持的特征重组动力学依赖于现有生物合成基因簇内的进化遗传变化，而不是简单地水平获取新的遗传元件或途径。最近，协同进化的地理镶嵌理论(GMC)提出了宏观生物的协同进化理论，该理论考虑了地理和局部适应如何塑造协同进化动力学。在这里，我们在一个古老的共生系统中测试GMC，在这个共生系统中，蚂蚁无齿蚂蚁在类似于人类耕作的农业系统中培养真菌。这些品种被真菌Ecovopsis寄生。蚂蚁保持共生放线菌，其抗生素特性有助于对抗Ecovopsis感染。这种抗生素共生关系已经持续了数千万年，这引发了如何在这些时间尺度上保持抗生素效力的问题。我们的研究在细菌防御性共生和多方共生框架中测试GMC。结果表明，这种多组分共生体系符合GMC，并证明该理论适用于微生物和间接共生体-共生体的相互作用。
The geographic mosaic theory of coevolution (GMC) posits that coevolutionary dynamics go beyond local coevolution and are comprised of the following three components: geographic selection mosaics, coevolutionary hot spots, and trait remixing. It is unclear whether the GMC applies to bacteria, as horizontal gene transfer and cosmopolitan dispersal may violate theoretical assumptions. Here, we test key GMC predictions in an antibiotic-producing bacterial symbiont (genus Pseudonocardia) that protects the crops of neotropical fungus-farming ants (Apterostigma dentigerum) from a specialized pathogen (genus Escovopsis). We found that Pseudonocardia antibiotic inhibition of common Escovopsis pathogens was elevated in A. dentigerum colonies from Panama compared to those from Costa Rica. Furthermore, a Panama Canal Zone population of Pseudonocardia on Barro Colorado Island (BCI) was locally adapted, whereas two neighboring populations were not, consistent with a GMC-predicted selection mosaic and a hot spot of adaptation surrounded by areas of maladaptation. Maladaptation was shaped by incongruent Pseudonocardia-Escovopsis population genetic structure, whereas local adaptation was facilitated by geographic isolation on BCI after the flooding of the Panama Canal. Genomic assessments of antibiotic potential of 29 Pseudonocardia strains identified diverse and unique biosynthetic gene clusters in BCI strains despite low genetic diversity in the core genome. The strength of antibiotic inhibition was not correlated with the presence/absence of individual biosynthetic gene clusters or with parasite location. Rather, biosynthetic gene clusters have undergone selective sweeps, suggesting that the trait remixing dynamics conferring the long-term maintenance of antibiotic potency rely on evolutionary genetic changes within already-present biosynthetic gene clusters and not simply on the horizontal acquisition of novel genetic elements or pathways.IMPORTANCE Recently, coevolutionary theory in macroorganisms has been advanced by the geographic mosaic theory of coevolution (GMC), which considers how geography and local adaptation shape coevolutionary dynamics. Here, we test GMC in an ancient symbiosis in which the ant Apterostigma dentigerum cultivates fungi in an agricultural system analogous to human farming. The cultivars are parasitized by the fungus Escovopsis. The ants maintain symbiotic actinobacteria with antibiotic properties that help combat Escovopsis infection. This antibiotic symbiosis has persisted for tens of millions of years, raising the question of how antibiotic potency is maintained over these time scales. Our study tests the GMC in a bacterial defensive symbiosis and in a multipartite symbiosis framework. Our results show that this multipartite symbiotic system conforms to the GMC and demonstrate that this theory is applicable in both microbes and indirect symbiont-symbiont interactions.