Ultrastructural and microspectrophotometric characterization of multiple species of cyanobacterial photosymbionts coexisting in the colonial ascidian<i>Trididemnum clinides</i>(Tunicata, Ascidiacea, Didemnidae)

Hirose, Euichi; Uchida, Hiroko; Murakami, Akio

doi:10.1080/09670260802710269

Cited by 20 publications

(22 citation statements)

References 34 publications

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“…Calothrix was also identified by Sanger sequencing of 16S PCR clone libraries. Filamentous cyanobacteria have previously been observed in Prochloron-bearing didemnids on several occasions, but not from L. patella (23)(24)(25)(26)(27)(28)(29). A few eukaryotic microbes, such as diatoms and dinoflagellates, were observed in L2 but not in L1 (Fig.…”

Section: Resultsmentioning

confidence: 85%

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Complex microbiome underlying secondary and primary metabolism in the tunicate- Prochloron symbiosis

Donia

Fricke

Partensky

et al. 2011

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

137

175

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The relationship between tunicates and the uncultivated cyanobacterium Prochloron didemni has long provided a model symbiosis. P. didemni is required for survival of animals such as Lissoclinum patella and also makes secondary metabolites of pharmaceutical interest. Here, we present the metagenomes, chemistry, and microbiomes of four related L. patella tunicate samples from a wide geographical range of the tropical Pacific. The remarkably similar P. didemni genomes are the most complex so far assembled from uncultivated organisms. Although P. didemni has not been stably cultivated and comprises a single strain in each sample, a complete set of metabolic genes indicates that the bacteria are likely capable of reproducing outside the host. The sequences reveal notable peculiarities of the photosynthetic apparatus and explain the basis of nutrient exchange underlying the symbiosis. P. didemni likely profoundly influences the lipid composition of the animals by synthesizing sterols and an unusual lipid with biofuel potential. In addition, L. patella also harbors a great variety of other bacterial groups that contribute nutritional and secondary metabolic products to the symbiosis. These bacteria possess an enormous genetic potential to synthesize new secondary metabolites. For example, an antitumor candidate molecule, patellazole, is not encoded in the genome of Prochloron and was linked to other bacteria from the microbiome. This study unveils the complex L. patella microbiome and its impact on primary and secondary metabolism, revealing a remarkable versatility in creating and exchanging small molecules.ascidian | metagenomics | photosynthesis | natural products

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Section: Resultsmentioning

confidence: 85%

“…P. didemni thus allows didemnid ascidians to thrive in nutrient-poor, light-rich environments of the tropics. Didemnids have also been found to contain other types of microbes, but unlike P. didemni, without extensive in vivo functional studies (21)(22)(23)(24)(25)(26)(27)(28)(29).…”

mentioning

confidence: 99%

Complex microbiome underlying secondary and primary metabolism in the tunicate- Prochloron symbiosis

Donia

Fricke

Partensky

et al. 2011

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

137

175

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“…The slower dynamics of O 2 in this layer is probably the result of light screening by cyanobacteria in the upper test and the Prochloron layer. Both zones of cyanobacteria have been observed before and the tunic is known to harbor the cyanobacterium Synechocystis trididemni and other cyanobacteria with special pigmentation (Lafargue and Duclaux, 1979; Kott, 1984; Cox et al, 1985; Hirose et al, 2009b; López-Legentil et al, 2011). López-Legentil et al (2011) found Chl d -containing Acaryochloris cells in the unic of other didemnid ascidians on mangrove roots in the Bahamas but we have not found any evidence for Chl d in the unic of L .…”

Section: Discussionmentioning

confidence: 99%

Microenvironmental Ecology of the Chlorophyll b-Containing Symbiotic Cyanobacterium Prochloron in the Didemnid Ascidian Lissoclinum patella

et al. 2012

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The discovery of the cyanobacterium Prochloron was the first finding of a bacterial oxyphototroph with chlorophyll (Chl) b, in addition to Chl a. It was first described as Prochloron didemni but a number of clades have since been described. Prochloron is a conspicuously large (7–25 μm) unicellular cyanobacterium living in a symbiotic relationship, primarily with (sub-) tropical didemnid ascidians; it has resisted numerous cultivation attempts and appears truly obligatory symbiotic. Recently, a Prochloron draft genome was published, revealing no lack of metabolic genes that could explain the apparent inability to reproduce and sustain photosynthesis in a free-living stage. Possibly, the unsuccessful cultivation is partly due to a lack of knowledge about the microenvironmental conditions and ecophysiology of Prochloron in its natural habitat. We used microsensors, variable chlorophyll fluorescence imaging and imaging of O2 and pH to obtain a detailed insight to the microenvironmental ecology and photobiology of Prochloron in hospite in the didemnid ascidian Lissoclinum patella. The microenvironment within ascidians is characterized by steep gradients of light and chemical parameters that change rapidly with varying irradiances. The interior zone of the ascidians harboring Prochloron thus became anoxic and acidic within a few minutes of darkness, while the same zone exhibited O2 super-saturation and strongly alkaline pH after a few minutes of illumination. Photosynthesis showed lack of photoinhibition even at high irradiances equivalent to full sunlight, and photosynthesis recovered rapidly after periods of anoxia. We discuss these new insights on the ecological niche of Prochloron and possible interactions with its host and other microbes in light of its recently published genome and a recent study of the overall microbial diversity and metagenome of L. patella.

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“…These mostly include other cyanobacteria, 32-36 but also reports about other types of bacteria, especially proteobacteria. 37-40 In the course of sequencing the P. didemni genome, we obtained an immense amount of data concerning other bacteria as well.…”

Section: Didemnid Houses For Bacteriamentioning

confidence: 99%

Origin and Variation of Tunicate Secondary Metabolites

et al. 2012

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Ascidians (tunicates) are rich sources of structurally elegant, pharmaceutically potent secondary metabolites and more recently, potential biofuels. It has been demonstrated that some of these compounds are made by symbiotic bacteria and not by the animals themselves, and for a few other compounds evidence exists supporting a symbiotic origin. In didemnid ascidians, compounds are highly variable even in apparently identical animals. Recently, we have explained this variation at the genomic and metagenomic levels and have applied the basic scientific findings to drug discovery and development. This review discusses what is currently known about the origin and variation of symbiotically derived metabolites in ascidians, focusing on Family Didemnidae, where most research has occurred. Applications of our basic studies are also described.

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Ultrastructural and microspectrophotometric characterization of multiple species of cyanobacterial photosymbionts coexisting in the colonial ascidianTrididemnum clinides(Tunicata, Ascidiacea, Didemnidae)

Cited by 20 publications

References 34 publications

Complex microbiome underlying secondary and primary metabolism in the tunicate- Prochloron symbiosis

Complex microbiome underlying secondary and primary metabolism in the tunicate- Prochloron symbiosis

Microenvironmental Ecology of the Chlorophyll b-Containing Symbiotic Cyanobacterium Prochloron in the Didemnid Ascidian Lissoclinum patella

Origin and Variation of Tunicate Secondary Metabolites

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