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Evolution of metabolic capabilities and molecular features of diplonemids, kinetoplastids, and euglenids.
BMC Biology ( IF 4.4 ) Pub Date : 2020-03-02 , DOI: 10.1186/s12915-020-0754-1
Anzhelika Butenko 1, 2 , Fred R Opperdoes 3 , Olga Flegontova 1, 2 , Aleš Horák 1, 4 , Vladimír Hampl 5 , Patrick Keeling 6 , Ryan M R Gawryluk 7 , Denis Tikhonenkov 6, 8 , Pavel Flegontov 1, 2, 9 , Julius Lukeš 1, 4
Affiliation  

BACKGROUND The Euglenozoa are a protist group with an especially rich history of evolutionary diversity. They include diplonemids, representing arguably the most species-rich clade of marine planktonic eukaryotes; trypanosomatids, which are notorious parasites of medical and veterinary importance; and free-living euglenids. These different lifestyles, and particularly the transition from free-living to parasitic, likely require different metabolic capabilities. We carried out a comparative genomic analysis across euglenozoan diversity to see how changing repertoires of enzymes and structural features correspond to major changes in lifestyles. RESULTS We find a gradual loss of genes encoding enzymes in the evolution of kinetoplastids, rather than a sudden decrease in metabolic capabilities corresponding to the origin of parasitism, while diplonemids and euglenids maintain more metabolic versatility. Distinctive characteristics of molecular machines such as kinetochores and the pre-replication complex that were previously considered specific to parasitic kinetoplastids were also identified in their free-living relatives. Therefore, we argue that they represent an ancestral rather than a derived state, as thought until the present. We also found evidence of ancient redundancy in systems such as NADPH-dependent thiol-redox. Only the genus Euglena possesses the combination of trypanothione-, glutathione-, and thioredoxin-based systems supposedly present in the euglenozoan common ancestor, while other representatives of the phylum have lost one or two of these systems. Lastly, we identified convergent losses of specific metabolic capabilities between free-living kinetoplastids and ciliates. Although this observation requires further examination, it suggests that certain eukaryotic lineages are predisposed to such convergent losses of key enzymes or whole pathways. CONCLUSIONS The loss of metabolic capabilities might not be associated with the switch to parasitic lifestyle in kinetoplastids, and the presence of a highly divergent (or unconventional) kinetochore machinery might not be restricted to this protist group. The data derived from the transcriptomes of free-living early branching prokinetoplastids suggests that the pre-replication complex of Trypanosomatidae is a highly divergent version of the conventional machinery. Our findings shed light on trends in the evolution of metabolism in protists in general and open multiple avenues for future research.

中文翻译:

二氢萘酮类,动质体和uglenidids的代谢能力和分子特征的演变。

背景技术裸藻纲动物是一个具有丰富的进化多样性历史的原生生物群体。它们包括二倍体,可以说是海洋浮游性真核生物中物种最多的进化枝。锥虫病,是医学和兽医学上臭名昭著的寄生虫;和自由生活的丑角。这些不同的生活方式,尤其是从自由生活向寄生虫的转变,可能需要不同的代谢能力。我们对整个真核动物多样性进行了比较基因组分析,以了解不断变化的酶组成和结构特征如何与生活方式的重大变化相对应。结果我们发现,在运动质体的进化过程中,编码酶的基因逐渐丢失,而不是与寄生虫起源相对应的代谢能力突然下降,而二氢萘酮类和延胡索类则保持更多的代谢多功能性。在其自由生活的亲戚中还发现了以前被认为对寄生性动质体特异的分子机器,如动植物和复制前复合体的显着特征。因此,我们认为它们代表的是祖先状态,而不是派生状态,直到现在。我们还发现了系统中古代冗余的证据,例如依赖NADPH的硫醇氧化还原。仅Euglena属拥有原定存在于euglenozoan共同祖先中的基于锥虫硫磷,谷胱甘肽和硫氧还蛋白的系统的组合,而门的其他代表却丢失了这些系统中的一两个。最后,我们确定了自由活动的动质体和纤毛虫之间特定代谢能力的收敛损失。尽管此观察结果需要进一步检查,但它表明某些真核细胞系易导致关键酶或整个途径的这种趋同丧失。结论代谢能力的丧失可能与运动质体中寄生生活方式的改变无关,并且高度分散的(或非常规的)动粒机制可能不限于该原生生物。来自自由生活的早期分支的原生质体的转录组的数据表明,锥虫科的复制前复合体是常规机械的高度不同的版本。
更新日期:2020-04-22
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