In:
Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, Vol. 108, No. 51 ( 2011-12-20)
Abstract:
These results reveal that L. patella is not merely a simple combination of a photoautotroph ( P. didemni ), i.e., an organism that carries out photosynthesis, and a filter-feeding animal. Instead, diverse bacteria interact in a complex way to define the rich primary and secondary metabolism of the holobiont. Although they are rare, patellazoles have been found in ascidians from Australia to Fiji during the past 30 years, and therefore, interaction with these other bacteria probably represents a stable association of partners beyond P. didemni . This study provides unique insights into the metabolic integration in a chordate model system and should impact discovery and development of biofuels and pharmaceutical natural products. By comparing the chemical composition of whole host–symbiont assemblages with the gene content of Prochloron genomes, we found that the major holobiont lipids (e.g., fats and cholesterol) are probably derived from P. didemni , including potential biofuels. However, we found that a few rare samples contained extremely potent anticancer lead compounds, patellazoles, which were not produced by P. didemni . Because of this, we reasoned that bacteria other than P. didemni might also contribute to the chemistry and metabolism of the host animal. By further examining the symbiotic microbiome and the ascidian genome of L. patella , we found a rich diversity of bacteria with an unprecedented variety and abundance of biosynthetic genes for natural products, including patellazoles. The complete set of metabolic genes, the remarkable photosynthetic apparatus, and the lack of nitrogen fixation persist in all four P. didemni genomes examined in this study. The genomes were remarkably similar to each other. This high level of genetic similarity, combined with the lack of genome streamlining, strongly suggests that Prochloron has a free-living stage in its life cycle and that, during this stage, cells may be transported over long distances, contributing to a homogenization of the population ( 5 ). The first near-complete genome sequence of P. didemni was obtained from L. patella from Palau. With approximately 6 million base pairs, this is the most complex genome assembly obtained to date from environmental samples. Typically, in symbiotic bacteria, the genome decays so that they can no longer live outside their host. However, in the case of P. didemni , no such streamlining was observed. Instead, we found that the genetic makeup of P. didemni seemingly comprises all metabolic genes present in free-living bacteria. We also found features that help explain its metabolic integration with the host. For example, based on the genome sequence, we determined that P. didemni can recycle the animal's waste nitrogen products. Contrary to expectation, P. didemni does not have the potential to fix nitrogen, and the necessary genes were not found in the ascidians. P. didemni has a complete photosynthetic machinery, providing a wealth of organic carbon compounds to his host. The set of pigments and sunscreen compounds synthesized by P. didemni is particularly well adapted to harvest blue light and to efficiently resist high light and UV stress that characterize shallow waters in which its ascidian host preferentially thrives. In an effort to better understand this model symbiosis, we performed an extensive study of the inner microbial flora of the didemnid ascidian L. patella . Animals from several locations were compared by an integrated set of genome-analysis techniques that allowed us to explore the complex association between the animal P. didemni and an extremely diverse set of other bacteria constituting this holobiont (the animal and its symbiotic partners). The P. didemni bacteria were previously shown to provide the animals with critical reduced carbon and nitrogen compounds, enabling the hosts to thrive in nutrient-poor coral reef environments ( 3 ). P. didemni also synthesizes toxic secondary metabolites that are pharmaceutical lead compounds and that are the major soluble constituents of the animal ( 4 ). P. didemni exchanges biosynthetic genes across its population, providing each animal with a different suite of secondary metabolites. Ascidians are a group of filter-feeding tunicates (commonly called sea squirts), which constitute a major component of the ecology of the ocean floor and which contain numerous small molecules important to pharmaceutical development ( 1 , 2 ). Like man, ascidians are chordate animals, and they house one of the best-studied cases of metabolic integration in the symbiosis between chordates and a bacterium. Specifically, a family of ascidians known as didemnids house a type of symbiotic bacterium, the cyanobacterium Prochloron didemni , that has never been stably cultivated. We used a suite of genetic analyses and chemical methods to investigate this symbiotic phenomenon between the didemnid ascidian Lissoclinum patella and the cyanobacterium P. didemni ( 3 ) ( Fig. P1 ). Through this approach, we unveiled the genomic basis of this symbiosis and discovered a unique set of gene products that might be useful in developing pharmaceuticals and biofuels. We also found a diverse and unexpected suite of cooccurring bacteria that contribute to the chemistry and metabolism of this multipartner symbiosis. Taken together, this work provides a comprehensive overview of the impact of symbiotic bacteria on a ubiquitous group of marine invertebrates that thrives in shallow tropical waters.
Type of Medium:
Online Resource
ISSN:
0027-8424
,
1091-6490
DOI:
10.1073/pnas.1111712108
Language:
English
Publisher:
Proceedings of the National Academy of Sciences
Publication Date:
2011
detail.hit.zdb_id:
209104-5
detail.hit.zdb_id:
1461794-8
SSG:
11
SSG:
12
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