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Synergism between the Black Queen effect and the proteomic constraint on genome size reduction in the photosynthetic picoeukaryotes.

ABSTRACT: The photosynthetic picoeukaryotes (PPEs) comprise a rare example of free-living eukaryotes that have undergone genome reduction. Here, we examine a duality in the process; the proposed driver of genome reduction (the Black Queen hypothesis, BQH), and the resultant impact of genome information loss (the Proteomic Constraint hypothesis, PCH). The BQH predicts that some metabolites may be shared in the open ocean, thus driving loss of redundant metabolic pathways in individual genomes. In contrast, the PCH predicts that as the information content of a genome is reduced, the total mutation load is also reduced, leading to loss of DNA repair genes due to the resulting reduction in selective constraint. Consistent with the BQH, we observe that biosynthetic pathways involved with soluble metabolites such as amino acids and carotenoids are preferentially lost from the PPEs, in contrast to biosynthetic pathways involved with insoluble metabolites, such as lipids, which are retained. Consistent with the PCH, a correlation between proteome size and the number of DNA repair genes, and numerous other informational categories, is observed. While elevated mutation rates resulting from the loss of DNA repair genes have been linked to reduced effective population sizes in intracellular bacteria, this remains to be established. This study shows that in microbial species with large population sizes, an underlying factor in modulating their DNA repair capacity appears to be information content.

SUBMITTER: Derilus D

PROVIDER: S-EPMC7265537 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:As the key contributor to plankton biomass and nutrient cycling in aquatic ecosystems, photosynthetic picoeukaryotes (PPEs) have been recently investigated in freshwater ecosystems. However, the limited access to remote areas creates challenges for PPE sample preservation before sorting and counting by flow cytometry (FCM) in the laboratory. Here, we explored the effects of different preservation methods on the PPE community by combining FCM sorting and high-throughput sequencing. Our results showed that dimethyl sulfoxide (DMSO) cryoprotection could destroy the fluorescence and cell structure of the PPEs, making the subsequent FCM analysis and sorting difficult. Aldehyde fixation maintained the PPE fluorescence, and the fixed samples were of sufficient quality for abundance analysis and sorting by FCM. However, the sequencing results showed that, after preservation by aldehydes, the proportion of PPEs dramatically decreased to approximately 10%, in comparison to 90% in the fresh samples, and the sequences of Ascomycota significantly increased. In contrast, preservation with Pluronic F68 (F68) not only could maintain the PPE abundance close to the initial value but also could keep the PPE community similar to that in the fresh samples over a storage time of 6 months. Thus, F68 cryopreservation is a suitable preservation method for PPE communities from freshwater lakes. IMPORTANCE PPEs contribute significantly to primary productivity in freshwater ecosystems. The combination of FCM sorting and high-throughput sequencing has been shown to be a powerful approach and can largely improve our view of the PPE diversity. However, the water samples could not be counted and sorted immediately after sampling from many lakes due to the inaccessibility of FCM in the field. Thus, the comparison of different preservation methods that allow subsequent analysis of the community structure by high-throughput sequencing is an urgent need. Our results indicated that F68 cryopreservation could maintain the PPE abundance close to the initial value and keep the community similar to that in the fresh samples over a storage time of 6 months.

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Synergism between the Black Queen effect and the proteomic constraint on genome size reduction in the photosynthetic picoeukaryotes.

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