Gene loss through pseudogenization contributes to the ecological diversification of a generalist Roseobacter lineage

Abstract

Ecologically relevant genes generally show patchy distributions among related bacterial genomes. This is commonly attributed to lateral gene transfer, whereas the opposite mechanism—gene loss—has rarely been explored. Pseudogenization is a major mechanism underlying gene loss, and pseudogenes are best characterized by comparing closely related genomes because of their short life spans. To explore the role of pseudogenization in microbial ecological diversification, we apply rigorous methods to characterize pseudogenes in the 279 newly sequenced Ruegeria isolates of the globally abundant Roseobacter group collected from two typical coastal habitats in Hong Kong, the coral Platygyra acuta and the macroalga Sargassum hemiphyllum. Pseudogenes contribute to ~16% of the accessory genomes of these strains. Ancestral state reconstruction reveals that many pseudogenization events are correlated with ancestral niche shifts. Specifically, genes related to resource scavenging and energy acquisition were often pseudogenized when roseobacters inhabiting carbon-limited and energy-poor coral skeleton switched to other resource-richer niches. For roseobacters inhabiting the macroalgal niches, genes for nitrogen regulation and carbohydrate utilization were important but became dispensable upon shift to coral skeleton where nitrate is abundant but carbohydrates are less available. Whereas low-energy-demanding secondary transporters are more favorable in coral skeleton, ATP-driven primary transporters are preferentially kept in the energy-replete macroalgal niches. Moreover, a large proportion of these families mediate organismal interactions, suggesting their rapid losses by pseudogenization as a potential response to host and niche shift. These findings illustrate an important role of pseudogenization in shaping genome content and driving ecological diversification of marine roseobacters.

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Fig. 1: The sampling information and phylogenomic analysis of the 279 isolates.
Fig. 2: Schematic illustration of pseudogene identification and ancestral states reconstruction.
Fig. 3: Overview of the pseudogenes in the 279 newly sequenced Ruegeria genomes.
Fig. 4: Examples of mapping pseudogenization/back events with niche shifts.
Fig. 5: A summary of the interpretation of pseudogenization and back events of the genetic traits in the Ruegeria isolates during different types of niche shifts.

Data availability

The 279 genome sequences released in this study have been deposited at the NCBI GenBank database under PRJNA593724 and PRJNA596594. The genome accession number of each isolate is shown in Supplementary Dataset S1. The full list of the identified pseudogenes is shown in Supplementary Dataset S5.

Code availability

Codes used to generate the results are available at https://doi.org/10.6084/m9.figshare.12545984.

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Acknowledgements

We thank Professor ANG Put On Jr. for providing the coral samples and LEUNG Yu Hin for assisting in macroalgal sample collection. We also thank FENG Xiaoyuan and LIAO Tianhua for assistance in bioinformatics analysis. This work was supported by the Shenzhen Science and Technology Committee (JCYJ20180508161811899), the National Natural Science Foundation of China (41776129), the Hong Kong Research Grants Council General Research Fund (14163917), the Hong Kong Environment and Conservation Fund (15/2016), the Hong Kong Research Grants Council Area of Excellence Scheme (AoE/M-403/16), and the Direct Grant of CUHK (4053437, 4053257, and 3132809).

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Chu, X., Li, S., Wang, S. et al. Gene loss through pseudogenization contributes to the ecological diversification of a generalist Roseobacter lineage. ISME J (2020). https://doi.org/10.1038/s41396-020-00790-0

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