Institute of Parasitology, Biology Centre, Czech Academy of Sciences, Branišovská, Branišovská 1160/31, 2, České Budějovice, 370 05, Czech Republic.
Department of Plant Biology and Biotechnology, Faculty of Biotechnology and Horticulture, University of Agriculturein Krakow, 29 Listopada Ave. 54, Kraków, 31-425, Poland.
BMC Biol. 2024 Sep 27;22(1):217. doi: 10.1186/s12915-024-02013-w.
Diplomonads are anaerobic flagellates classified within Metamonada. They contain both host-associated commensals and parasites that reside in the intestinal tracts of animals, including humans (e.g., Giardia intestinalis), as well as free-living representatives that inhabit freshwater and marine anoxic sediments (e.g., Hexamita inflata). The evolutionary trajectories within this group are particularly unusual as the free-living taxa appear to be nested within a clade of host-associated species, suggesting a reversal from host-dependence to a secondarily free-living lifestyle. This is thought to be an exceedingly rare event as parasites often lose genes for metabolic pathways that are essential to a free-living life strategy, as they become increasingly reliant on their host for nutrients and metabolites. To revert to a free-living lifestyle would require the reconstruction of numerous metabolic pathways. All previous studies of diplomonad evolution suffered from either low taxon sampling, low gene sampling, or both, especially among free-living diplomonads, which has weakened the phylogenetic resolution and hindered evolutionary insights into this fascinating transition.
We sequenced transcriptomes from 1 host-associated and 13 free-living diplomonad isolates; expanding the genome scale data sampling for diplomonads by roughly threefold. Phylogenomic analyses clearly show that free-living diplomonads form several branches nested within endobiotic species. Moreover, the phylogenetic distribution of genes related to an endobiotic lifestyle suggest their acquisition at the root of diplomonads, while traces of these genes have been identified in free-living diplomonads as well. Based on these results, we propose an evolutionary scenario of ancestral and derived lifestyle transitions across diplomonads.
Free-living taxa form several clades nested within endobiotic taxa in our phylogenomic analyses, implying multiple transitions between free-living and endobiotic lifestyles. The evolutionary history of numerous virulence factors corroborates the inference of an endobiotic ancestry of diplomonads, suggesting that there have been several reversals to a free-living lifestyle. Regaining host independence may have been facilitated by a subset of laterally transferred genes. We conclude that the extant diversity of diplomonads has evolved from a non-specialized endobiont, with some taxa becoming highly specialized parasites, others becoming free-living, and some becoming capable of both free-living and endobiotic lifestyles.
双滴虫是后生动物门的一类厌氧鞭毛虫。它们包含既存在于动物肠道中的共生寄生物，也包含寄生虫，包括人类（例如，肠贾第虫），以及存在于淡水和海洋缺氧沉积物中的自由生活代表（例如，膨胀六鞭毛虫）。该群体内的进化轨迹特别不寻常，因为自由生活的分类群似乎嵌套在一个与宿主相关物种的分支内，这表明它们从对宿主的依赖转变为次要的自由生活方式。这被认为是一种非常罕见的事件，因为寄生虫通常会失去对其自由生活策略至关重要的代谢途径的基因，因为它们越来越依赖宿主获取营养和代谢物。要恢复自由生活方式，需要重建许多代谢途径。以前所有关于双滴虫进化的研究都存在分类群采样低或基因采样低，或两者兼而有之的问题，尤其是在自由生活的双滴虫中，这削弱了系统发育分辨率，并阻碍了对这种迷人转变的进化见解。
我们从 1 种宿主相关和 13 种自由生活的双滴虫分离株中测序了转录组；使双滴虫的基因组规模数据采样扩大了大约三倍。系统基因组分析清楚地表明，自由生活的双滴虫形成了几个分支，嵌套在内生种内。此外，与内生生活方式相关的基因的系统发生分布表明它们是在双滴虫的根部获得的，而这些基因的痕迹也在自由生活的双滴虫中被识别出来。基于这些结果，我们提出了一个跨越双滴虫的祖先和衍生生活方式转变的进化情景。
在我们的系统基因组分析中，自由生活的分类群形成了几个嵌套在内生分类群内的分支，这意味着自由生活和内生生活方式之间发生了多次转变。大量毒力因子的进化历史证实了双滴虫的内生起源的推断，表明已经有几次向自由生活方式的逆转。重新获得对宿主的独立性可能是由一组侧向转移基因促成的。我们得出的结论是，现存的双滴虫多样性是从非特化的内共生体进化而来的，一些类群成为高度特化的寄生虫，另一些成为自由生活的，还有一些类群能够同时适应自由生活和内共生生活。
