A Highly Polymorphic Receptor Governs Many Distinct Self-Recognition Types within the Myxococcales Order

A Highly Polymorphic Receptor Governs Many Distinct Self-Recognition Types within the Myxococcales Order
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DOI:
10.1128/mbio.02751-18
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发表时间:
2019-01-01
期刊:
影响因子:
6.4
通讯作者:
Wall, Daniel
Wall, Daniel
中科院分区:
生物学1区
文献类型:
--
作者:
Cao, Pengbo;Wei, Xueming;Wall, Daniel

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自我认知是许多群居生物体社会性的基础。在细菌中,细胞使用各种策略来识别亲属以形成社会群体,并在某些情况下转变为多细胞生命。一种策略依赖于编码可变表型标签(“绿胡子”)的单个遗传位点来识别其他标签持有者。此前,我们发现了一种名为 TraA 的多态性细胞表面受体,它通过社会细菌黄粘球菌中的同型相互作用来指导自我识别。 TraA 的识别导致细胞资源在称为外膜交换 (OME) 的过程中共享。 traA 操纵子中的第二个基因 traB 也是 OME 所必需的,但不参与识别。我们之前对 TraA 的研究仅在密切相关的 M. xanthus 分离株中识别出六个识别组。在这里,我们假设野生分离株中 traA 多态性的数量以及因此识别的多样性要大得多。为了检验这一假设,我们将 TraA 表征的范围扩大到粘球菌目。从粘球菌目三个亚目的基因组序列中,我们鉴定了 90 个 traA 直向同源物。 traAB 位点的序列分析和功能表征表明,OME 在不同的粘细菌分类群中得到了很好的维护。重要的是,TraA 直向同源物在其可变域(赋予自我识别选择性的区域)内具有高度多态性。我们通过实验定义了 10 个不同的识别组,并根据系统发育和实验分析,预测 90 个 traA 等位基因中有超过 60 个识别组。总而言之,我们的研究结果揭示了一个广泛存在的绿胡子基因座,它介导粘球菌目的自我识别的多样性。重要性 许多生物物种通过使用不同的机制来区分自我和异己。高等动物通过复杂的过程来识别近亲,这些过程通常涉及五种感觉、认知和学习,而一些微生物仅通过单个基因位点的活动来实现自我识别。在这里,我们描述了粘细菌中控制自然群体内细胞间识别的单个基因座 traA。我们发现 traA 在粘球菌目中广泛存在。 TraA 在不同的粘细菌分离株中具有高度多态性,这种多态性决定了自我识别的选择性。通过生物信息学和实验分析,我们表明 traA 控制着粘球菌目中的许多不同的识别群。该报告提供了一个例子,其中单个基因座影响自然种群广泛系统发育范围的社会识别。
Self-recognition underlies sociality in many group-living organisms. In bacteria, cells use various strategies to recognize kin to form social groups and, in some cases, to transition into multicellular life. One strategy relies on a single genetic locus that encodes a variable phenotypic tag ("greenbeard") for recognizing other tag bearers. Previously, we discovered a polymorphic cell surface receptor called TraA that directs self-identification through homotypic interactions in the social bacterium Myxococcus xanthus. Recognition by TraA leads to cellular resource sharing in a process called outer membrane exchange (OME). A second gene in the traA operon, traB, is also required for OME but is not involved in recognition. Our prior studies of TraA identified only six recognition groups among closely related M. xanthus isolates. Here we hypothesize that the number of traA polymorphisms and, consequently, the diversity of recognition in wild isolates are much greater. To test this hypothesis, we expand the scope of TraA characterization to the order Myxococcales. From genomic sequences within the three suborders of Myxococcales, we identified 90 traA orthologs. Sequence analyses and functional characterization of traAB loci suggest that OME is well maintained among diverse myxobacterial taxonomic groups.Importantly, TraA orthologs are highly polymorphic within their variable domain, the region that confers selectivity in self-recognition. We experimentally defined 10 distinct recognition groups and, based on phylogenetic and experimental analyses, predicted >60 recognition groups among the 90 traA alleles. Taken together, our findings revealed a widespread greenbeard locus that mediates the diversity of self-recognition across the order Myxococcales. IMPORTANCE Many biological species distinguish self from nonself by using different mechanisms. Higher animals recognize close kin via complex processes that often involve the five senses, cognition, and learning, whereas some microbes achieve self-recognition simply through the activity of a single genetic locus. Here we describe a single locus, traA, in myxobacteria that governs cell-cell recognition within natural populations. We found that traA is widespread across the order Myxococcales. TraA is highly polymorphic among diverse myxobacterial isolates, and such polymorphisms determine selectivity in self-recognition. Through bioinformatic and experimental analyses, we showed that traA governs many distinct recognition groups within Myxococcales. This report provides an example in which a single locus influences social recognition across a wide phylogenetic range of natural populations.