Prophages in Lactobacillus reuteri Are Associated with Fitness Trade-Offs but Can Increase Competitiveness in the Gut Ecosystem

Prophages in Lactobacillus reuteri Are Associated with Fitness Trade-Offs but Can Increase Competitiveness in the Gut Ecosystem
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DOI:
10.1128/aem.01922-19
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发表时间:
2020-01-01
影响因子:
4.4
通讯作者:
Van Pijkeren, Jan-Peter
Van Pijkeren, Jan-Peter
中科院分区:
生物学2区
文献类型:
--
作者:
Oh, Jee-Hwan;Lin, Xiaoxi B.;Van Pijkeren, Jan-Peter

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肠道微生物群含有多种噬菌体群体,其主要来源于溶原菌,溶原菌是在其基因组中含有休眠的细菌。虽然肠道生态系统中细菌的多样性越来越好地表征,但关于细菌如何促进宿主细菌的进化和生态的知识有限。在这里,我们表明,生物活性的前噬菌体广泛分布在肠道共生菌罗伊氏乳杆菌的遗传多样性菌株。几乎所有的人类和啮齿动物来源的菌株,但不到一半的测试菌株的猪源,含有活性的前噬菌体,这表明不同的角色,在主机特定的谱系的进化。为了深入了解L. reuteri等,我们发展了L. reuteri菌株6475作为模型研究其致病性。给小鼠灌胃L. reuteri 6475在整个肠道中产生活性的大肠杆菌,在远端结肠中检测到的数量最多。recA的失活消除了体内噬菌体的产生,这表明SOS应答的激活驱动了肠道中的噬菌体产生。在常规小鼠中,噬菌体生产降低了细菌适应性,因为与缺乏前噬菌体的突变体相比,更少的野生型细菌在肠道运输中存活。然而,在gnotobiotic小鼠中,噬菌体生产提供了L。reuteri与一个敏感的主机的竞争优势。总的来说,我们发现,原噬菌体的存在,虽然与健身权衡,可以是有利的肠道共生体杀死竞争对手的菌株在其肠道niche.IMPORTANCE来源于溶原菌的噬菌体是丰富的肠道微生物。目前,机制的知识是缺乏对生态后果的原噬菌体运输,但必须解释丰富的溶原细胞在肠道。细菌肠道共生体罗伊氏乳杆菌的广泛筛选显示,生物活性的原噬菌体广泛分布在这个物种中。L. reuteri 6475在整个小鼠肠道中产生噬菌体,但是噬菌体的产生与溶原菌的适应性降低有关。然而,噬菌体生产在与非溶原性的乳酸杆菌菌株的直接竞争中提供了竞争优势。对这些病毒敏感的reuteri。这种竞争增加与适应性权衡的结合为溶原菌在肠道生态系统中的主导地位以及溶原菌如何与敏感宿主共存提供了潜在的解释。
The gut microbiota harbors a diverse phage population that is largely derived from lysogens, which are bacteria that contain dormant phages in their genome. While the diversity of phages in gut ecosystems is getting increasingly well characterized, knowledge is limited on how phages contribute to the evolution and ecology of their host bacteria. Here, we show that biologically active prophages are widely distributed in phylogenetically diverse strains of the gut symbiont Lactobacillus reuteri. Nearly all human- and rodent-derived strains, but less than half of the tested strains of porcine origin, contain active prophages, suggesting different roles of phages in the evolution of host-specific lineages. To gain insight into the ecological role of L. reuteri phages, we developed L. reuteri strain 6475 as a model to study its phages. After administration to mice, L. reuteri 6475 produces active phages throughout the intestinal tract, with the highest number detected in the distal colon. Inactivation of recA abolished in vivo phage production, which suggests that activation of the SOS response drives phage production in the gut. In conventional mice, phage production reduces bacterial fitness as fewer wild-type bacteria survive gut transit compared to the mutant lacking prophages. However, in gnotobiotic mice, phage production provides L. reuteri with a competitive advantage over a sensitive host. Collectively, we uncovered that the presence of prophages, although associated with a fitness trade-off, can be advantageous for a gut symbiont by killing a competitor strain in its intestinal niche.IMPORTANCE Bacteriophages derived from lysogens are abundant in gut microbiomes. Currently, mechanistic knowledge is lacking on the ecological ramifications of prophage carriage yet is essential to explain the abundance of lysogens in the gut. An extensive screen of the bacterial gut symbiont Lactobacillus reuteri revealed that biologically active prophages are widely distributed in this species. L. reuteri 6475 produces phages throughout the mouse intestinal tract, but phage production is associated with reduced fitness of the lysogen. However, phage production provides a competitive advantage in direct competition with a nonlysogenic strain of L. reuteri that is sensitive to these phages. This combination of increased competition with a fitness trade-off provides a potential explanation for the domination of lysogens in gut ecosystem and how lysogens can coexist with sensitive hosts.