The luggage hypothesis: Comparisons of two phototrophic hosts with nitrogen-fixing cyanobacteria and implications for analogous life strategies for kleptoplastids/secondary symbiosis in dinoflagellates

Wouters, Johanna; Raven, John A.; Minnhagen, Susanna; Janson, Sven

doi:10.1007/s13199-009-0020-3

Cited by 17 publications

(4 citation statements)

References 96 publications

(88 reference statements)

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“…containing the nucleus, mitochondria, Golgi apparatuses, etc.) as a permanent endosymbiont by synchronizing the endosymbiont cell division to the host cell cycle (Wouters et al, 2009;Imanian et al, 2010). A similar situation is also observed in other eukaryotic groups.…”

supporting

confidence: 68%

Mechanism of Plastid Division: From a Bacterium to an Organelle

Miyagishima

2011

Plant Physiology

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supporting

confidence: 68%

Mechanism of Plastid Division: From a Bacterium to an Organelle

Miyagishima

2011

Plant Physiology

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“…In certain cases, the kleptoplast divides in accord with dinoflagellate cell division and is inherited for a number of generations (6). A few dinoflagellate species maintain a eukaryotic algal unicell (i.e., containing a nucleus, mitochondria, Golgi apparatus, and so forth) as a permanent endosymbiont by synchronizing the endosymbiont cell division to the host cell cycle (7,8). There also are eukaryotes that possess permanent cyanobacterial endosymbionts, such as Paulinella chromatophora (Cercozoa).…”

mentioning

confidence: 99%

Chloroplast division checkpoint in eukaryotic algae

Sumiya

Fujiwara

Era

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Chloroplasts evolved from a cyanobacterial endosymbiont. It is believed that the synchronization of endosymbiotic and host cell division, as is commonly seen in existing algae, was a critical step in establishing the permanent organelle. Algal cells typically contain one or only a small number of chloroplasts that divide once per host cell cycle. This division is based partly on the S-phase-specific expression of nucleus-encoded proteins that constitute the chloroplast-division machinery. In this study, using the red alga Cyanidioschyzon merolae, we show that cell-cycle progression is arrested at the prophase when chloroplast division is blocked before the formation of the chloroplastdivision machinery by the overexpression of Filamenting temperaturesensitive (Fts) Z2-1 (Fts72-1), but the cell cycle progresses when chloroplast division is blocked during division-site constriction by the overexpression of either FtsZ2-1 or a dominant-negative form of dynamin-related protein 5B (DRP5B). In the cells arrested in the prophase, the increase in the cyclin B level and the migration of cyclin-dependent kinase B (CDKB) were blocked. These results suggest that chloroplast division restricts host cell-cycle progression so that the cell cycle progresses to the metaphase only when chloroplast division has commenced. Thus, chloroplast division and host cell-cycle progression are synchronized by an interactive restriction that takes place between the nucleus and the chloroplast. In addition, we observed a similar pattern of cell-cycle arrest upon the blockage of chloroplast division in the glaucophyte alga Cyanophora paradoxa, raising the possibility that the chloroplast division checkpoint contributed to the establishment of the permanent organelle.chloroplast division | algal cell cycle | Cyanidioschyzon merolae | Cyanophora paradoxa C hloroplasts trace their origin to a primary endosymbiotic event that took place more than a billion years ago, a process in which an ancestral cyanobacterium became integrated into a previously nonphotosynthetic eukaryote. The ancient alga that resulted from this primary endosymbiotic event evolved into the Glaucophyta (glaucophyte algae), Rhodophyta (red algae), and Viridiplantae (green algae, streptophyte algae, and land plants), which together are grouped as the Plantae (sensu stricto) or Archaeplastida. After these primitive green and red algae had become established, chloroplasts then spread into other eukaryote lineages through secondary endosymbiotic events in which a red or green alga became integrated into previously nonphotosynthetic eukaryotes (1).The continuity of chloroplasts has been maintained for more than a billion years. The majority of algae (both unicellular and multicellular, with both possessing chloroplasts of primary and secondary endosymbiotic origin) have one or at most only a few chloroplasts per cell. Thus, chloroplast division is synchronized with the host cell cycle so that the chloroplast divides before cytokinesis and is thus transmitted into each daughter cell ...

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“…The lack of permanent endosymbionts can also be explained by the “luggage” hypothesis proposed by Wouters et al (2009) on the pages of “Symbiosis” nearly seven years ago. It states that as long as symbionts or plastid donors are present and abundant in the host environment, the most favoured host strategy will be preying on them.…”

Section: Acquired Phototrophy In the Light Of The “Luggage” Hypothesismentioning

confidence: 96%

“…On the other hand, the fewer symbionts or plastid donors in the environment, the more likely the host is to hold them as permanent luggage. The hosts that are able to maintain endosymbionts or kleptoplastids for a longer time are favoured, for example, in dynamic environments or when the host finds itself in a new environment (see next section for an example; Wouters et al 2009). …”

Section: Acquired Phototrophy In the Light Of The “Luggage” Hypothesismentioning

confidence: 99%

Cymbomonas tetramitiformis - a peculiar prasinophyte with a taste for bacteria sheds light on plastid evolution

Gagat

Mackiewicz

2016

Symbiosis

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Cymbomonas tetramitiformis is a peculiar green alga that unites in one cell the abilities of photosynthesis and phagocytosis, which makes it a very useful model for the study of the evolution of plastid endosymbiosis. We have pondered over this issue and propose an evolutionary scenario of trophic strategies in eukaryotes, including primary and secondary plastid endosymbioses. C. tetramitiformis is a prototroph, just like the common ancestor of Archaeplastida was, and can synthesize most small organic molecules contrary to other eukaryotic phagotrophs, e.g. some metazoans, amoebozoans, and ciliates, which have not evolved tight endosymbiotic relationships. In order to establish a permanent photosynthetic endosymbiont they do not have to become prototrophs, but have to acquire the genes necessary for plastid retention via horizontal (including endosymbiotic) gene transfer. Such processes occurred successfully in the ancestors of eukaryotes with permanent secondary plastids and thus led to their great diversification. The preservation of phagocytosis in Cymbomonas (and some other prasinophytes as well) seems to result from nutrient deficiency in their oligotrophic habitats. This forces them to supplement their diet with phagocytized prey, in contrasts to the thecate amoeba Paulinella chromatophora, which also successfully transformed cyanobacteria into permanent organelles. Although Paulinella endosymbionts were acquired very recently in comparison to primary plastids, Paulinella has lost the ability to phagocytose, most probably due to the fact that it inhabits nutrient-rich environments, which renders the phagotrophy nonessential.

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The luggage hypothesis: Comparisons of two phototrophic hosts with nitrogen-fixing cyanobacteria and implications for analogous life strategies for kleptoplastids/secondary symbiosis in dinoflagellates

Cited by 17 publications

References 96 publications

Mechanism of Plastid Division: From a Bacterium to an Organelle

Mechanism of Plastid Division: From a Bacterium to an Organelle

Chloroplast division checkpoint in eukaryotic algae

Cymbomonas tetramitiformis - a peculiar prasinophyte with a taste for bacteria sheds light on plastid evolution

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