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A microbial eukaryote with a unique combination of purple bacteria and green algae as endosymbionts.

ABSTRACT: Oxygenic photosynthesizers (cyanobacteria and eukaryotic algae) have repeatedly become endosymbionts throughout evolution. In contrast, anoxygenic photosynthesizers (e.g., purple bacteria) are exceedingly rare as intracellular symbionts. Here, we report on the morphology, ultrastructure, lifestyle, and metagenome of the only "purple-green" eukaryote known. The ciliate Pseudoblepharisma tenue harbors green algae and hundreds of genetically reduced purple bacteria. The latter represent a new candidate species of the Chromatiaceae that lost known genes for sulfur dissimilation. The tripartite consortium is physiologically complex because of the versatile energy metabolism of each partner but appears to be ecologically specialized as it prefers hypoxic sediments. The emergent niche of this complex symbiosis is predicted to be a partial overlap of each partners' niches and may be largely defined by anoxygenic photosynthesis and possibly phagotrophy. This purple-green ciliate thus represents an extraordinary example of how symbiosis merges disparate physiologies and allows emergent consortia to create novel ecological niches.

SUBMITTER: Munoz-Gomez SA

PROVIDER: S-EPMC8195481 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: The order Rickettsiales comprises gram-negative obligate intracellular bacteria (also called rickettsias) that are mainly associated with arthropod hosts. This group is medically important because it contains human-pathogenic species that cause dangerous diseases. Until now, there has been no report of non-phagotrophic photosynthetic eukaryotes, such as green plants, harboring rickettsias. METHODOLOGY/PRINCIPAL FINDINGS: We examined the bacterial endosymbionts of two freshwater volvocalean green algae: unicellular Carteria cerasiformis and colonial Pleodorina japonica. Epifluorescence microscopy using 4'-6-deamidino-2-phenylindole staining revealed the presence of endosymbionts in all C. cerasiformis NIES-425 cells, and demonstrated a positive correlation between host cell size and the number of endosymbionts. Strains both containing and lacking endosymbionts of C. cerasiformis (NIES-425 and NIES-424) showed a >10-fold increase in cell number and typical sigmoid growth curves over 192 h. A phylogenetic analysis of 16 S ribosomal (r)RNA gene sequences from the endosymbionts of C. cerasiformis and P. japonica demonstrated that they formed a robust clade (hydra group) with endosymbionts of various non-arthropod hosts within the family Rickettsiaceae. There were significantly fewer differences in the 16 S rRNA sequences of the rickettsiacean endosymbionts between C. cerasiformis and P. japonica than in the chloroplast 16 S rRNA or 18 S rRNA of the host volvocalean cells. Fluorescence in situ hybridization demonstrated the existence of the rickettsiacean endosymbionts in the cytoplasm of two volvocalean species. CONCLUSIONS/SIGNIFICANCE: The rickettsiacean endosymbionts are likely not harmful to their volvocalean hosts and may have been recently transmitted from other non-arthropod organisms. Because rickettsias are the closest relatives of mitochondria, incipient stages of mitochondrial endosymbiosis may be deduced using both strains with and without C. cerasiformis endosymbionts.

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A microbial eukaryote with a unique combination of purple bacteria and green algae as endosymbionts.

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