Chloroplast history clarified by the criterion of light-harvesting complex
Introduction
Photosynthetic machinery in green protists, algae, and plants is collectively known as plastids. The origin of plastids surmises the endosymbiotic association between mitochondrial protist, as a senior (larger size) partner, and either cyanobacterium or green protist, as a junior (smaller size) partner (Bhattacharya and Medlin, 1995; Douglas, 1998; Tomitani et al., 1999). Thus, plastids are of at least two types: (1) simple plastids, or chloroplasts − direct descendants of cyanobacteria, (2) complex plastids which indirectly descended from degenerative green protists, and consist of the chloroplast core escorted by rudimentary host cell organelles: plasma membrane, eukaryotic 80S ribosomes, and, in most complicated cases, a residual nucleus termed the nucleomorph (Cavalier-Smith, 2002; Keeling, 2004). In other words, plastids originated via primary endosymbiosis and secondary endosymbiosis, respectively.
Bacterial nature of mitochondria and chloroplasts was initially proclaimed in general outline by K. Mereschkowsky (1905), and in 1924 by B. Kozo-Polyansky (see: Kozo-Polyansky, 2010). Then, the remarkable insight gave way to an elaborate hypothesis by I. Wallin (1927) and L. Margulis (see: Gray, 2017). Finally it took shape of a conventional theory reliably corroborated by molecular biology data (Nelissen et al., 1995; Cavalier-Smith, 2000). In particular, chloroplasts have been incorporated into the cyanobacterial tree based on the fundamental molecular phylogeny marker − rrn operon (Dagan et al., 2013). Chloroplast diversity and ancestry can be also traced with the rpoС and psbA genes, rbc operon, and other molecular criteria of prime importance (Moreira et al., 2000). Among these criteria is also light-harvesting complex (LHC) (Durnford et al., 1999; Wolfe et al., 1994). LHC competence is a prerequisite of partnership between host eukaryote and pre-chloroplast, and it makes the partnership more consolidated. LHC pigment and protein moieties underlie light acclimation strategies in ancient and modern biosphere (Averina et al., 2018, 2019).
In this review, the criterion of LHC is applied to chloroplast origin and diversity. In particular, ancient cyanobacterium possessing tandem antenna (encoded by the cbp genes and the pbp genes, correspondingly), and defined as a prochlorophyte, is argued to be chloroplast ancestor.
Section snippets
Cyanobacteria: general features
Fossilized cyanobacteria are among the eldest micropaleontology records (Schopf, 2000). According to molecular paleontology data, the phylum Cyanobacteria embraces the phototrophic class Oxyphotobacteria, and two non-phototrophic classes − Melainabacteria and Sericytochromatia (Soo et al., 2017). Oxyphotobacteria (cyanobacteria in the narrow sense of the word) excrete triplet dioxygen − the byproduct of unique H2O-dehydrogenase reaction. Oxygenic photosynthesis is often accompanied with
Simple plastids (chloroplasts)
Chloroplasts are present in (1) glaucophytes (Glaucocystophyceae), (2) red algae (Rhodophyceae), (3) green algae (Chlorophyceae and Charophyceae), and green plants (Plantae). Glaucophytes represent a small group of nine freshwater protist genera. Their photosynthetic endosymbionts termed cyanelles, or cyanoplasts, have rudimentary cell wall, and thus represent an intermediate stage in chloroplast evolution (Bhattacharya and Schmidt, 1997). Their LHC is represented by the phycobilisome (PBS).
Chlorophylls
Chlorophylls are designated alphabetically, from a to f, according to the order of their discovery. The absence of a ‘Chl e’ is explained by unfounded reports on this pigment in certain green algae. In contrast to ample data on LHC pigments in chloroplasts, the evidence on b- and c-type chlorophylls, Chl d, and Chl f in cyanobacteria is scarce (Miyashita et al., 1996; Larkum et al., 2018; Averina et al., 2019).
While the majority of cyanobacteria contain Chl a as their only chlorophyll, the
Chlorophyll/protein light-harvesting complexes
Сhlorophyll-containing LHC have been preferentially studied in chlorobionts (Chlorophyceae, Euglenophyceae, and green plants (Jansson, 1994; La Roche et al., 1996). Core antenna and peripheral antenna of PSI and PSII are shown to contain three domain 22−26 kDa polypeptides from the CAB superfamily. In particular, PSI core antenna is composed of two copies of the Lhca1−4 CAB proteins, respectively; on the whole, they bind 100 Chl a/b, 24 lutein, and 9 violaxanthin molecules. In its turn, PSII
Prochlorophytes as chloroplast ancestry
The observed diversity of prochlorophytes is surprisingly small (Pinevich et al., 2012). At the same time, some of them possess the photosystems perfectly adapted to light quality that makes these cyanobacteria most abundant phototrophs on Earth (MacGregor-Chatwin et al., 2019). Besides, in the evolutionary retrospect, they could have played a key role in chloroplast history.
There are a limited number of hypotheses which concretize a presumable chloroplast ancestor. Thus, one of early
Conclusion
Based on the final thesis, and taking into account the data compiled in this review, it can be attempted to partially rehabilitate the early hypothesis by Ralph Lewin (1981b). In other words, one can draw the conclusion that prochlorophytes represents the key player in chloroplast history.
As in other molecular phylogeny analyses, the rrn operon helps to place chloroplasts onto the bacterial dendrogram. Chloroplast ancestry and diversity can be further traced with the rpoС and psbA genes, rbc
Funding information
The work was supported by the Russian Foundation for Fundamental Research (Russia), project no. 20-04-00020.
Declaration of competing interest
The author declares no conflict of interests.
Acknowledgement
I thank anonymous reviewers for their contribution to the peer review of this work.
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