Biotic Host–Pathogen Interactions As Major Drivers of Plastid Endosymbiosis

Cenci, Ugo; Bhattacharya, Debashish; Weber, Andreas P.M.; Colleoni, Christophe; Subtil, Agathe; Ball, Steven

doi:10.1016/j.tplants.2016.12.007

Cited by 44 publications

(41 citation statements)

References 59 publications

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“…Rather, we have to assume many repeated endosymbiotic events with cyanobacteria, chlamydiae, green bacteria, and others, if we still use endosymbiotic explanation. There are discussions about the role of chlamydiae, working with cyanobacteria to establish chloroplasts (Cenci et al 2017;Domman et al 2015), but the problem might not be limited to chlamydiae. Do we need to keep the endosymbiotic explanation?…”

Section: Historical Considerations On the Origin Of Endosymbiotic Theorymentioning

confidence: 99%

Complex origins of chloroplast membranes with photosynthetic machineries: multiple transfers of genes from divergent organisms at different times or a single endosymbiotic event?

Sato

2019

J Plant Res

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The paradigm "cyanobacterial origin of chloroplasts" is currently viewed as an established fact. However, we may have to reconsider the origin of chloroplast membranes, because membranes are not replicated by their own. It is the genes for lipid biosynthetic enzymes that are inherited. In the current understandings, these enzymes became encoded by the nuclear genome as a result of endosymbiotic gene transfer from the endosymbiont. However, we previously showed that many enzymes involved in the synthesis of chloroplast peptidoglycan and glycolipids did not originate from cyanobacteria. Here I present results of comprehensive phylogenetic analysis of chloroplast enzymes involved in fatty acid and lipid biosynthesis, as well as additional chloroplast components related to photosynthesis and gene expression. Four types of phylogenetic relationship between chloroplast enzymes (encoded by the chloroplast and nuclear genomes) and cyanobacterial counterparts were found: type 1, chloroplast enzymes diverged from inside of cyanobacterial clade; type 2, chloroplast and cyanobacterial enzymes are sister groups; type 3, chloroplast enzymes originated from homologs of bacteria other than cyanobacteria; type 4, chloroplast enzymes diverged from eukaryotic homologs. Estimation of evolutionary distances suggested that the acquisition times of chloroplast enzymes were diverse, indicating that multiple gene transfers accounted for the chloroplast enzymes analyzed. Based on the results, I try to relax the tight logic of the endosymbiotic origin of chloroplasts involving a single endosymbiotic event by proposing alternative hypotheses. The hypothesis of host-directed chloroplast formation proposes that glycolipid synthesis ability had been acquired by the eukaryotic host before the acquisition of chloroplast ribosomes. Chloroplast membrane system could have been provided by the host, whereas cyanobacteria contributed to the genes for the genetic and photosynthesis systems, at various times, either before or after the formation of chloroplast membranes. The origin(s) of chloroplasts seems to be more complicated than the single event of primary endosymbiosis.

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Section: Historical Considerations On the Origin Of Endosymbiotic Theorymentioning

confidence: 99%

Complex origins of chloroplast membranes with photosynthetic machineries: multiple transfers of genes from divergent organisms at different times or a single endosymbiotic event?

Sato

2019

J Plant Res

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“…These observations have led to the ‘ménage à trois’ hypothesis (MATH) to explain the origin of plastids. In this scenario, a Chlamydiales ancestor evolved from a pathogenic to symbiotic lifestyle, protecting the cyanobacterium in its inclusion vesicle (Ball et al ., ; Cenci et al ., ). Although the MATH remains controversial, largely as a result of issues associated with ‘deep time’ gene phylogenies and the unresolved role of HGT in eukaryote evolution (Dagan et al ., ; Ball et al ., 2016a), its complexity reflects well‐established biotic interactions.…”

Section: Endosymbiosismentioning

confidence: 97%

Biotic interactions as drivers of algal origin and evolution

et al. 2017

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Contents 670 I. 671 II. 671 III. 676 IV. 678 678 References 678 SUMMARY: Biotic interactions underlie life's diversity and are the lynchpin to understanding its complexity and resilience within an ecological niche. Algal biologists have embraced this paradigm, and studies building on the explosive growth in omics and cell biology methods have facilitated the in-depth analysis of nonmodel organisms and communities from a variety of ecosystems. In turn, these advances have enabled a major revision of our understanding of the origin and evolution of photosynthesis in eukaryotes, bacterial-algal interactions, control of massive algal blooms in the ocean, and the maintenance and degradation of coral reefs. Here, we review some of the most exciting developments in the field of algal biotic interactions and identify challenges for scientists in the coming years. We foresee the development of an algal knowledgebase that integrates ecosystem-wide omics data and the development of molecular tools/resources to perform functional analyses of individuals in isolation and in populations. These assets will allow us to move beyond mechanistic studies of a single species towards understanding the interactions amongst algae and other organisms in both the laboratory and the field.

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“…Interestingly, their evolutionary origin can neither be traced back to cyanobacteria (cyanobacteria, however, do possess NTT-HEAT domain fusion proteins [41]), nor to the eukaryotic non-photosynthetic ancestor of algae and plants with primary plastids. This gave rise to hypotheses of horizontal transfer of NTT genes from ancestors of infectious intracellular bacteria to the ancestor of photosynthetic eukaryotes during or preceding endosymbiosis with the plastid ancestor, known as the "menage a trois" hypothesis [6,69,70]. This hypothesis is based on the manipulation of the host glycogen metabolism by extant chlamydiae, and on phylogenies of a number of genes.…”

Section: Evolutionary Implications Of the Distribution Of Ntts Acrossmentioning

confidence: 99%

“…One aspect of the "menage a trois" hypothesis is that it postulates that chlamydial NTTs allowed the cyanobacteria to persist in the host cell after they lost the ability to accumulate and consume their own glycogen [70]. Here, the patchy distribution of NTTs in the tree of life offers a strong point in favor of the "menage a trois" hypothesis: single domain NTTs are neither found in cyanobacteria nor in the vast majority of non-photosynthetic free-living eukaryotes.…”

Section: Evolutionary Implications Of the Distribution Of Ntts Acrossmentioning

confidence: 99%

Nucleotide Transport and Metabolism in Diatoms

Gruber

Haferkamp

2019

Biomolecules

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Plastids, organelles that evolved from cyanobacteria via endosymbiosis in eukaryotes, provide carbohydrates for the formation of biomass and for mitochondrial energy production to the cell. They generate their own energy in the form of the nucleotide adenosine triphosphate (ATP). However, plastids of non-photosynthetic tissues, or during the dark, depend on external supply of ATP. A dedicated antiporter that exchanges ATP against adenosine diphosphate (ADP) plus inorganic phosphate (Pi) takes over this function in most photosynthetic eukaryotes. Additional forms of such nucleotide transporters (NTTs), with deviating activities, are found in intracellular bacteria, and, surprisingly, also in diatoms, a group of algae that acquired their plastids from other eukaryotes via one (or even several) additional endosymbioses compared to algae with primary plastids and higher plants. In this review, we summarize what is known about the nucleotide synthesis and transport pathways in diatom cells, and discuss the evolutionary implications of the presence of the additional NTTs in diatoms, as well as their applications in biotechnology.Cyanobacteria store the photosynthesized carbohydrates in the bacterial cytoplasm in the form of glycogen and use these stores for the generation of energy via respiration, which allows them to tide over conditions in which photosynthesis is not possible, for instance in the absence of light [17]. In contrast, in the majority of photosynthetic eukaryotes, storage carbohydrates are located outside of the plastid stroma and hence outside of the former cyanobacterial cytosol. However, green algae and plants are a notable exception, because their starch metabolism has secondarily been re-allocated to the plastid [18,19]. Consequently, whenever photosynthesis is insufficient to meet the ATP demand, the plastid needs to be supplied with this energy currency from other sources. The corresponding ATP production can take place in mitochondria (through respiration), or in the cytosol (through substrate-level phosphorylation). In photosynthetic eukaryotes, plastidic ATP uptake is catalyzed by specific solute transport proteins called nucleotide transporters (NTTs) [20][21][22]. These NTTs are present in the inner envelope membrane, where they act as antiporters, exchanging ATP against adenosine diphosphate (ADP) plus inorganic phosphate (Pi) [20,23] (Figure 1a).

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Biotic Host–Pathogen Interactions As Major Drivers of Plastid Endosymbiosis

Cited by 44 publications

References 59 publications

Complex origins of chloroplast membranes with photosynthetic machineries: multiple transfers of genes from divergent organisms at different times or a single endosymbiotic event?

Complex origins of chloroplast membranes with photosynthetic machineries: multiple transfers of genes from divergent organisms at different times or a single endosymbiotic event?

Biotic interactions as drivers of algal origin and evolution

Nucleotide Transport and Metabolism in Diatoms

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