Host-Microbe Interactions in the Chemosynthetic Riftia pachyptila Symbiosis
Host-Microbe Interactions in the Chemosynthetic Riftia pachyptila Symbiosis
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DOI：
10.1128/mbio.02243-19
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发表时间：
2019-11-01
期刊：
影响因子：
6.4
通讯作者：
Markert, Stephanie
中科院分区：
文献类型：
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作者：
Hinzke, Tjorven;Kleiner, Manuel;Markert, Stephanie
深海管虫Riftia pachyptila缺乏消化系统，但完全依赖细菌内共生体获得营养。虽然共生体已经在分子水平上进行了详细的研究，但由于缺乏序列信息，这种分析无法用于动物宿主。为了确定宿主-共生体相互作用机制，我们因此对Riftia转录组进行了测序，这是在能量丰富和能量有限的条件下，对含共生体与无共生体的组织进行比较元蛋白质组学分析的基础。我们的研究结果表明，代谢相互作用包括共生体的营养分配到主机的共生体消化和底物转移到共生体丰富的主机蛋白质。我们还提出，Riftia通过保护细菌免受氧化损伤来维持其共生体，同时还发挥共生体种群控制作用。类真核共生蛋白可能促进细胞内共生体的持久性。能量限制显然导致共生体生物量减少和共生体消化增加。我们的研究提供了前所未有的见解宿主-微生物相互作用，塑造这种高效的共生关系。重要性所有动物都与微生物有关;因此，宿主-微生物相互作用对地球上的生命至关重要。然而，我们对这些相互作用的分子基础知之甚少。因此，我们研究了深海Riftia pachyptila共生，一种模式协会，其中管虫宿主仅与一种内共生细菌类型相关，并完全依赖于这种硫氧化共生体的营养。使用元蛋白质组学方法，我们确定了代谢相互作用过程，如两个伙伴之间的底物转移，以及用于维持共生平衡的相互作用，例如，宿主控制共生体种群的努力或调节这些宿主努力的共生体策略。我们认为，这些相互作用是互惠互利的动物微生物协会的基本原则。
The deep-sea tubeworm Riftia pachyptila lacks a digestive system but completely relies on bacterial endosymbionts for nutrition. Although the symbiont has been studied in detail on the molecular level, such analyses were unavailable for the animal host, because sequence information was lacking. To identify host-symbiont interaction mechanisms, we therefore sequenced the Riftia transcriptome, which served as a basis for comparative metaproteomic analyses of symbiont-containing versus symbiont-free tissues, both under energy-rich and energy-limited conditions. Our results suggest that metabolic interactions include nutrient allocation from symbiont to host by symbiont digestion and substrate transfer to the symbiont by abundant host proteins. We furthermore propose that Riftia maintains its symbiont by protecting the bacteria from oxidative damage while also exerting symbiont population control. Eukaryote-like symbiont proteins might facilitate intracellular symbiont persistence. Energy limitation apparently leads to reduced symbiont biomass and increased symbiont digestion. Our study provides unprecedented insights into host-microbe interactions that shape this highly efficient symbiosis.IMPORTANCE All animals are associated with microorganisms; hence, host-microbe interactions are of fundamental importance for life on earth. However, we know little about the molecular basis of these interactions. Therefore, we studied the deep-sea Riftia pachyptila symbiosis, a model association in which the tubeworm host is associated with only one phylotype of endosymbiotic bacteria and completely depends on this sulfur-oxidizing symbiont for nutrition. Using a metaproteomics approach, we identified both metabolic interaction processes, such as substrate transfer between the two partners, and interactions that serve to maintain the symbiotic balance, e.g., host efforts to control the symbiont population or symbiont strategies to modulate these host efforts. We suggest that these interactions are essential principles of mutualistic animal-microbe associations.