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Plastid Origin: Who, When and Why?

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Plastid Origin: Who, When and Why? Acta Societatis Botanicorum Poloniae INVITED REVIEW Acta Soc Bot Pol 83(4):281–289 DOI: 10.5586/asbp.2014.045 Received: 2014-11-20 Accepted: 2014-12-04 Published electronically: 2014-12-31 Plastid origin: who, when and why? Chuan Ku, Mayo Roettger, Verena Zimorski, Shijulal Nelson-Sathi, Filipa L. Sousa, William F. Martin* Institute of Molecular Evolution, Heinrich-Heine-University Düsseldorf, Universitätsstr. 1, 40225 Düsseldorf, Germany Abstract The origin of plastids is best explained by endosymbiotic theory, which dates back to the early 1900s. Three lines of evidence based on protein import machineries and molecular phylogenies of eukaryote (host) and cyanobacterial (endo- symbiont) genes point to a single origin of primary plastids, a unique and important event that successfully transferred two photosystems and oxygenic photosynthesis from prokaryotes to eukaryotes. The nature of the cyanobacterial lineage from which plastids originated has been a topic of investigation. Recent studies have focused on the branching position of the plastid lineage in the phylogeny based on cyanobacterial core genes, that is, genes shared by all cyanobacteria and plastids. These studies have delivered conflicting results, however. In addition, the core genes represent only a very small portion of cyanobacterial genomes and may not be a good proxy for the rest of the ancestral plastid genome. Information in plant nuclear genomes, where most genes that entered the eukaryotic lineage through acquisition from the plastid ancestor reside, suggests that heterocyst-forming cyanobacteria in Stanier’s sections IV and V are most similar to the plastid ancestor in terms of gene complement and sequence conservation, which is in agreement with models suggesting an important role of nitrogen fixation in symbioses involving cyanobacteria. Plastid origin is an ancient event that involved a prokaryotic symbiont and a eukaryotic host, organisms with different histories and genome evolutionary processes. The different modes of genome evolution in prokaryotes and eukaryotes bear upon our interpretations of plastid phylogeny. Keywords: cyanobacteria; endosymbiosis; evolution; gene transfer; genomics; organelle; photosynthesis; phylogeny Plastid origin: 110 years since Mereschkowsky With the availability of protein and DNA sequences, of which Mereschkowsky knew nothing, strong evidence had accu- Plastids are eukaryotic metabolic compartments re- mulated by the early 1980s that plastids originated through sponsible for photosynthesis [1] and a variety of metabolic endosymbiosis from cyanobacteria, rather than autogenously functions including the biosynthesis of amino acids [2], [16]. However, there have been recurrent suggestions, start- nucleotides [3], lipids [4], and cofactors [5]. The importance ing with Mereschkowsky [6] and tracing into the 1970’s [17], of plastids to photosynthetic lineages of eukaryotes cannot that there were several independent origins of plastids from be overstated. In 1905, Mereschkowsky proposed a fully cyanobacteria. Today it is widely, but not universally [18,19], articulated version of endosymbiotic theory positing that accepted that plastids had a single origin. The strongest plastids originated from cyanobacteria that came to reside evidence for that view is that the protein import machinery, as symbionts in eukaryotic cells [6,7]. The theory did not a good marker for endosymbiotic events [20], in the three make its way into mainstream biological thinking until it was lineages of Archaeplastida – eukaryotes with primary plastids revived in a synthesis by Margulis [8,9] that also incorpo- [21] – consists of homologous host-originated components rated Wallin’s [10] – and Paul Portier’s (published in French, [22–24], which would not be the case had plastids in those cited in Sapp [11]) – ideas about endosymbiotic theory for lineages arisen from independent cyanobacterial symbioses. mitochondrial origin, yet adorned by Margulis’ own sugges- Genomics has enriched our understanding of plastid tion of a spirochaete origin of flagella. The spirochaete story origin. We now know that the plastid genome has undergone never took hold, leaving endosymbiotic theory with three extreme reduction while leaving its imprints in the nuclear main players: the plastid, the mitochondrion, and its host, genome through endosymbiotic gene transfer [25,26] and which is now understood to be an archaeon [12]. Well into that plastids have spread across eukaryotes through symbiosis the 1970s, resistance to the concept of endosymbiosis for and become secondary and tertiary plastids [27]. Genomic the origin of plastids (and mitochondria) was stiff [13–15]. data also supports the case for a single plastid origin. Despite some concerns about incomplete sampling and phylogenetic artifacts [18], recent analyses from different groups, incor- * Corresponding author. Email: [email protected] porating improved phylogenetic algorithms and sampling of Handling Editor: Andrzej Bodył cyanobacteria, provide two lines of evidence, in addition to This is an Open Access article distributed under the terms of the Creative Commons Attribution 3.0 License (creativecommons.org/licenses/by/3.0/), which permits 281 redistribution, commercial and non-commercial, provided that the article is properly cited. © The Author(s) 2014 Published by Polish Botanical Society Ku et al. / Who, when and why of plastid origin the protein import machinery, for a monophyletic origin of some general trends regarding the relationships of extant plastids involving a single host lineage and a single cyano- cyanobacteria have emerged from studies based on rDNA bacterial lineage. (i) All plastids are monophyletic and nested or multiple protein-coding genes [30,32–34,38–43], which within the cyanobacterial clade [28–34]. (ii) Eukaryotes with are summarized as the backbone tree shown in Fig. 1. There primary plastids are monophyletic based on both nuclear is little dispute that the thylakoid-lacking genus Gloeobacter [29,35] and mitochondrial [36] genomes. (with which Aphanothece is possibly synonymous [40,44]) However, much is still left unknown about the origin of is the most basal lineage within cyanobacteria, whose clos- plastids. What is the cyanobacterial lineage most closely est relatives discovered so far are the nonphotosynthetic related to plastids? What was the ancestor of plastids like melainabacteria [43]. The other cyanobacteria can be fur- as it entered into the symbiotic relationship? What might ther divided into a basal clade of Synechococcus strains be the reasons that triggered this far-reaching event? Here (e.g., JA-2-3B), a clade of Synechococcus sp. PCC 7502 and we consider these aspects and recent advances on issues Pseudanabaena strains (e.g., PCC 7367), and a core clade concerning the when, who and why of plastid origin. consisting of the other taxa (Fig. 1). The core cyanobacteria contain the majority of the described species and strains and can be further divided into three groups: a clade of section When: early or late branching for the I taxa (e.g., Thermosynechococcus; this clade’s basal position plastid lineage within cyanobacteria? is not recovered in some analyses [31,38,39,41,43]), a clade of mixed section III and I taxa (including the fast-evolving Cyanobacteria are traditionally classified into five sections SynPro clade of Synechococcus and Prochlorococcus) and according to their morphological and developmental patterns finally a clade where all sections are represented, including [37]. Section I are unicellular cocci, section II are cocci that heterocyst-forming and true-branching taxa. aggregate, section III are filamentous, section IV are filamen- If we take the last common ancestor of the core cyano- tous with heterocysts, and section V are filamentous with bacteria as a reference point, much of the recent debate on true branching and heterocysts. That taxonomy does not, the closest extant cyanobacterial neighbor of the plastids is however, correspond to molecular phylogenetic groupings in about “early” (point “a” in Fig. 1 [30–33]) versus “late” (points any phylogeny reported so far. Although different molecular “b–e” in Fig. 1 [29,34,38,39,45,46]) plastid branching. Here phylogenies are often themselves mutually inconsistent, instead of “early origin” [47] or “deep origin” [30], the term Representative taxa Sections Groupings [37] [32,34] [30,33] [31,41] [42] Possible branching point of the plastid Chlorogloeopsis, Fischerella, lineage Scytonema hofmanni IV, V e B1 E1 Anabaena, Nodularia, Nostoc IV NOST-1 PNT c Lyngbya PCC 8106 Oscillatoria (PCC 6506 ...) Core cyanobacteria III Trichodesmium A OSC-2 Crocosphaera, Cyanothece (PCC E2 b d 8801 ...), Leptolyngbya PCC 7376, Microcystis, Pleurocapsa, Prochloron, I, II, III B2 SPM-3 SPM-3 Synechococcus PCC 7002 a Cyanobium Prochlorococcus I C1 Synechococcus (CC 9605 ...) SO-6 SynPro Synechococcus elongatus I C2 Leptolyngbya (PCC 6406, AC PCC 7375 ...) Synechococcus I, III C3 PHOR-7 LPP PCC 7335 Acaryochloris, Synechococcus PCC 6312, Cyanothece PCC I E UNIT(+) 7425, Thermosynechococcus Basal cyanobacteria Pseudanabaena Synechococcus PCC 7502 I, III F Synechococcus (JA-2-3B, JA-3-3Ab, PCC 7336 ...) I G GBACT Gloeobacter I Melainabacteria Fig. 1 Possible branching points of the plastid lineage in a consensus cyanobacterial tree based on molecular phylogenetic studies [29–34,38–40,42,43], showing section distribution [37] and groupings in different references. Dotted lines indicate a branching pattern not recovered in some
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