Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis

Abstract

The integration of foreign genetic information is central to the evolution of eukaryotes, as has been demonstrated for the origin of the Calvin cycle and of the heme and carotenoid biosynthesis pathways in algae and plants. For photosynthetic lineages, this coordination involved three genomes of divergent phylogenetic origins (the nucleus, plastid, and mitochondrion). Major hurdles overcome by the ancestor of these lineages were harnessing the oxygen-evolving organelle, optimizing the use of light, and stabilizing the partnership between the plastid endosymbiont and host through retargeting of proteins to the nascent organelle. Here we used protein similarity networks that can disentangle reticulate gene histories to explore how these significant challenges were met. We discovered a previously hidden component of algal and plant nuclear genomes that originated from the plastid endosymbiont: symbiogenetic genes (S genes). These composite proteins, exclusive to photosynthetic eukaryotes, encode a cyanobacteriumderived domain fused to one of cyanobacterial or another prokaryotic origin and have emerged multiple, independent times during evolution. Transcriptome data demonstrate the existence and expression of S genes across a wide swath of algae and plants, and functional data indicate their involvement in tolerance to oxidative stress, phototropism, and adaptation to nitrogen limitation. Our research demonstrates the "recycling" of genetic information by photosynthetic eukaryotes to generate novel composite genes, many of which function in plastid maintenance.gene fusion | endosymbiosis | photosynthesis | eukaryote evolution | novel gene origin T he genomes of the proteobacterium-derived mitochondrion and the cyanobacterium-derived plastid have undergone significant genome reduction due to outright gene loss or transfer to the nuclear genome (1, 2). Organelle gene loss by transfer to the nucleus is known as endosymbiotic gene transfer [EGT (a special form of horizontal gene transfer; HGT)] and has resulted in chimeric host nuclear genomes with, in the case of plastids, from ca. 200 to several thousand intact endosymbiont genes being relocated (3) (Fig. 1A). Plastid EGT has a long evolutionary history, extending back over a billion years in the case of primary plastid origin in the Archaeplastida (glaucophytes, red and green algae, and their sister group, plants) and several hundred million years for secondary plastids in groups such as diatoms, haptophytes, and dinoflagellates (4). A common fate for many nuclear-encoded organelle-derived proteins is to be targeted back to the compartment of origin via channels [i.e., translocons at the outer-and inner-envelope membrane of plastids and mitochondria (Toc/Tic and Tom/Tim, respectively)] to carry out organelle functions (5). Identification of EGT candidates generally relies on phylogenetic methods that use simultaneous alignment of colinear proteins sharing significant sequence similarity over all, or most, of their lengths to reconstruct the tree and its constituent ...

Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome

“…Thus, the chimeric origins of the ochrophyte plastid might have enabled the creation of syncretic proteins not found in the endosymbiont or host ancestors. We identified orthologues of seven chimeric proteins identified in this study within our dataset, underlining their importance for the establishment of the ochrophyte plastid (Figure 6, panel A) (Méheust et al, 2016).

10.7554/eLife.23717.031Figure 6.Origins of chimeric proteins in the ochrophyte plastid.(Panel A ) tabulates eight ancestral HPPGs containing domains of cyanobacterial and non-cyanobacterial origin, as previously identified (Méheust et al, 2016) that were inherited by the ochrophyte plastid, and two chimeric ancestral HPPGs which are probably of specific ochrophyte origin.

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“…We identified orthologues of seven chimeric proteins identified in this study within our dataset, underlining their importance for the establishment of the ochrophyte plastid (Figure 6, panel A) (Méheust et al, 2016).

10.7554/eLife.23717.031Figure 6.Origins of chimeric proteins in the ochrophyte plastid.(Panel A ) tabulates eight ancestral HPPGs containing domains of cyanobacterial and non-cyanobacterial origin, as previously identified (Méheust et al, 2016) that were inherited by the ochrophyte plastid, and two chimeric ancestral HPPGs which are probably of specific ochrophyte origin. (Panel B ) shows a complete tabulated list of all ancestral HPPGs (listed by identifier, with the predicted function given in brackets) in which at least one chimerism event between domains of red algal, green algal, aplastidic stramenopile, other eukaryotic, and prokaryotic origin was detected.

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No genome is an island: toward a 21st century agenda for evolution

“…As with mitochondria, conversion of the endosymbiotic bacterium into an organelle involved considerable DNA transfer to the nuclear genome. A number of nuclear‐encoded proteins important for plastid function have sequence signatures indicating cyanobacterial contributions to their evolution . In the Arabidopsis embryophyte nuclear genome, for example, it was found that ∼18% of the nuclear protein‐coding sequences came from Cyanobacteria …”

Phenotypic diversity within two toxic dinoflagellate genera: environmental and transcriptomic studies of species diversity in Alexandrium and Gambierdiscus

“…Furthermore, dinoflagellates have been shown to 'recycle' genetic material to regulate their plastid photosynthetic machinery (Méheust, Zelzion, Bhattacharya, Lopez, & Bapteste, 2016). In the case of the saxitoxin biosynthesis pathway, it's possible that genes from a HGT event between a cyanobacterium and a dinoflagellate are now being used not only to produce saxitoxin and its derivatives, but also may be used in other pathways.…”

“…Furthermore, endosymbiosis may be an even greater driver of HGT in dinoflagellates since they have been shown to incorporate an unusually high proportion of plastid genes to their nucleus, more so than many other eukaryotes (Archibald, 2009;Dorrell & Howe, 2015). Dinoflagellates also 'recycle' genetic material to regulate their plastid photosynthetic machinery from multiple sources which sometimes results in the fusion of domains from different organisms into chimeric sequences (Méheust et al, 2016). They also recycle genes for use in different pathways, resulting in at least one documented example of a hybrid metabolic pathway with components from different evolutionary origins (Bentlage, Rogers, Bachvaroff, & Delwiche, 2016).…”