Institute of Integrative Genome Biology, University of California, Riverside, Riverside, CA 92521, USA.
Department of Microbiology & Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA.
Curr Biol. 2023 Jul 24;33(14):2988-3001.e4. doi: 10.1016/j.cub.2023.06.081.
The capacity of beneficial microbes to compete for host infection-and the ability of hosts to discriminate among them-introduces evolutionary conflict that is predicted to destabilize mutualism. We investigated fitness outcomes in associations between legumes and their symbiotic rhizobia to characterize fitness impacts of microbial competition. Diverse Bradyrhizobium strains varying in their capacity to fix nitrogen symbiotically with a common host plant, Acmispon strigosus, were tested in full-factorial coinoculation experiments involving 28 pairwise strain combinations. We analyzed the effects of interstrain competition and host discrimination on symbiotic-interaction outcomes by relativizing fitness proxies to clonally infected and uninfected controls. More than one thousand root nodules of coinoculated plants were genotyped to quantify strain occupancy, and the Bradyrhizobium strain genome sequences were analyzed to uncover the genetic bases of interstrain competition outcomes. Strikingly, interstrain competition favored a fast-growing, minimally beneficial rhizobia strain. Host benefits were significantly diminished in coinoculation treatments relative to expectations from clonally inoculated controls, consistent with competitive interference among rhizobia that reduced both nodulation and plant growth. Competition traits appear polygenic, linked with inter-strain allelopathic interactions in the rhizosphere. This study confirms that competition among strains can destabilize mutualism by favoring microbes that are superior in colonizing host tissues but provide minimal benefits to host plants. Moreover, our findings help resolve the paradox that despite efficient host control post infection, legumes nonetheless encounter rhizobia that vary in their nitrogen fixation.
有益微生物争夺宿主感染的能力——以及宿主辨别它们的能力——引入了进化冲突,预计这会使共生关系不稳定。我们研究了豆科植物与其共生根瘤菌之间的适应结果,以描述微生物竞争对适应的影响。不同的布拉氏固氮菌菌株在与共同宿主植物 Acmispon strigosus 共生固氮的能力上存在差异,在涉及 28 对菌株组合的完全因子共接种实验中进行了测试。我们通过将适应度指标相对于克隆感染和未感染的对照进行相对化,分析了菌株间竞争和宿主辨别对共生相互作用结果的影响。对共接种植物的一千多个根瘤进行了基因型分析,以量化菌株占有率,并且分析了布拉氏固氮菌菌株的基因组序列,以揭示菌株间竞争结果的遗传基础。惊人的是,菌株间竞争有利于生长较快、益处最小的根瘤菌菌株。与从克隆接种对照中预期的相比,在共接种处理中宿主的收益明显减少,这与根瘤菌之间的竞争干扰一致,这种干扰减少了结瘤和植物生长。竞争特性似乎是多基因的,与根际中的菌株间化感相互作用有关。这项研究证实,菌株间的竞争可以通过有利于在定植宿主组织方面具有优势但对宿主植物提供最小益处的微生物来破坏共生关系。此外,我们的研究结果有助于解决一个悖论,即尽管在感染后宿主对微生物有高效的控制,但豆科植物仍然会遇到在固氮方面存在差异的根瘤菌。