Genomes of Novel Myxococcota Reveal Severely Curtailed Machineries for Predation and Cellular Differentiation

Genomes of Novel Myxococcota Reveal Severely Curtailed Machineries for Predation and Cellular Differentiation
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DOI:
10.1128/aem.01706-21
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发表时间:
2021-12-01
影响因子:
4.4
通讯作者:
Youssef, Noha H.
Youssef, Noha H.
中科院分区:
生物学2区
文献类型:
--
作者:
Murphy, Chelsea L.;Yang, R.;Youssef, Noha H.

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培养粘球菌主要是好氧土壤居民,其特点是高度协调的捕食和细胞分化能力。目前对厌氧非土壤生境中尚未培养的粘球菌知之甚少。我们分析了来自美国俄克拉荷马州缺氧淡水泉(Zodletone Spring)的粘球菌中代表一个新目的(o_JAFGXQ01)和一个新家族(f_JAFGIB 01)的基因组。与土壤中的粘球菌相比,厌氧粘球菌具有较小的基因组和较少数量的编码生物合成基因簇(BGC)、肽酶、单组分和双组分信号转导系统和转录调节因子的基因。对捕食和细胞分化至关重要的13种不同途径/过程的详细分析揭示了严重削减的机制,关键转录因子的同源物明显缺乏(例如,FruA和MrpC),外膜交换受体(TraA),以及大多数孢子形成特异性和A运动特异性基因。此外,基于一组634个提供社会生活方式信息的基因的机器学习方法预测了Zodletone Myxococcota的非社会行为。在代谢方面,Zodletone Myxococcota基因组缺乏有氧呼吸能力,但携带提示发酵、异化亚硝酸盐还原和异化硫酸盐还原(f_JAFGIB 01中)以获取能量的基因。我们建议,捕食和细胞分化代表了一个生态位的适应策略,大约5亿年前(Mya),在响应土壤的崛起作为一个独特的栖息地在地球上。重要意义的门粘球菌是一个共生一致的细菌谱系,表现出独特的社会特征。培养的粘球菌主要是好氧的土壤微生物,能够捕食和子实体的形成。然而,多个尚未培养的谱系内的粘球菌已经遇到了广泛的非土壤,主要是厌氧栖息地,和代谢能力,生理偏好,以及社会行为的能力,这样的谱系仍然不清楚。在这里,我们分析了从美国俄克拉荷马州缺氧淡水泉的宏基因组分析中回收的基因组,这些基因组代表了粘球菌门中新的、尚未培养的目和科。基因组似乎缺乏粘球菌基因组中遇到的社会行为的特征标志,并显示出一个显着较小的基因组大小和编码生物合成基因簇,肽酶,信号转导系统和转录调节因子的基因数量较少。通过对与粘球菌社会行为相关的13种途径进行详细的比较基因组分析,以及基于基因组组成预测社会行为的机器学习方法的实施,证实了这种社会能力的缺乏。在代谢上,这些新的粘球菌被预测为严格的厌氧菌,利用发酵、硝酸盐还原和不同的硫酸盐还原来获得能量。我们的研究结果突出了尚未培养的粘球菌内的代谢多样性的广泛模式,并表明捕食和子实体形成的粘球菌的进化已经发生在地球上的土壤形成作为一个独特的栖息地。
Cultured Myxococcota are predominantly aerobic soil inhabitants, characterized by their highly coordinated predation and cellular differentiation capacities. Little is currently known regarding yet-uncultured Myxococcota from anaerobic, nonsoil habitats. We analyzed genomes representing one novel order (o_JAFGXQ01) and one novel family (f_JAFGIB01) in the Myxococcota from an anoxic freshwater spring (Zodletone Spring) in Oklahoma, USA. Compared to their soil counterparts, anaerobic Myxococcota possess smaller genomes and a smaller number of genes encoding biosynthetic gene clusters (BGCs), peptidases, one- and two-component signal transduction systems, and transcriptional regulators. Detailed analysis of 13 distinct pathways/processes crucial to predation and cellular differentiation revealed severely curtailed machineries, with the notable absence of homologs for key transcription factors (e.g., FruA and MrpC), outer membrane exchange receptor (TraA), and the majority of sporulation-specific and A-motility-specific genes. Further, machine learning approaches based on a set of 634 genes informative of social lifestyle predicted a nonsocial behavior for Zodletone Myxococcota. Metabolically, Zodletone Myxococcota genomes lacked aerobic respiratory capacities but carried genes suggestive of fermentation, dissimilatory nitrite reduction, and dissimilatory sulfate-reduction (in f_JAFGIB01) for energy acquisition. We propose that predation and cellular differentiation represent a niche adaptation strategy that evolved circa 500 million years ago (Mya) in response to the rise of soil as a distinct habitat on Earth.IMPORTANCE The phylum Myxococcota is a phylogenetically coherent bacterial lineage that exhibits unique social traits. Cultured Myxococcota are predominantly aerobic soildwelling microorganisms that are capable of predation and fruiting body formation. However, multiple yet-uncultured lineages within the Myxococcota have been encountered in a wide range of nonsoil, predominantly anaerobic habitats, and the metabolic capabilities, physiological preferences, and capacity of social behavior of such lineages remain unclear. Here, we analyzed genomes recovered from a metagenomic analysis of an anoxic freshwater spring in Oklahoma, USA, that represent novel, yet-uncultured, orders and families in the Myxococcota. The genomes appear to lack the characteristic hallmarks for social behavior encountered in Myxococcota genomes and displayed a significantly smaller genome size and a smaller number of genes encoding biosynthetic gene clusters, peptidases, signal transduction systems, and transcriptional regulators. Such perceived lack of social capacity was confirmed through detailed comparative genomic analysis of 13 pathways associated with Myxococcota social behavior, as well as the implementation of machine learning approaches to predict social behavior based on genome composition. Metabolically, these novel Myxococcota are predicted to be strict anaerobes, utilizing fermentation, nitrate reduction, and dissimilarity sulfate reduction for energy acquisition. Our results highlight the broad patterns of metabolic diversity within the yet-uncultured Myxococcota and suggest that the evolution of predation and fruiting body formation in the Myxococcota has occurred in response to soil formation as a distinct habitat on Earth.