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. Photosynthetic picoeukaryotes (PPEs) are single celled eukaryotic algae of cell size less than 3 µm in diameter 1. Their individual cell size is much reduced compared to other eukaryotes, and comparable to Prochlorococcus and Synechococcus picocyanobacteria, which have also undergone cell size reduction (cell size <2 µm 2 ,). They are typically motile and found in the oceanic euphotic zone 3,4. Molecular 5 and metagenomic 6-9 analyses show that PPEs possess a global distribution. While factors which affect the distribution of PPEs are not well understood 3 , temperature and dissolved oxygen appear to have a role 8. There is evidence of the importance of PPEs in biogeochemical processes such as carbon fixation 6,10 , despite their low numerical abundance compared to cyanobacteria 10. The reduction in cell size of both marine PPEs and picocyanobacteria has occurred concomitantly with a reduction in genome size. These two groups of photosynthetic microbes represent rare examples of free-living organisms that have undergone reduction in genome size, however the evolutionary forces and environmental factors leading to genome reduction in these two lineages are not well understood 11,12. While these forces may be similar given their common habitat, it is unclear if they represent a case of convergent evolution, until the imperatives behind cell and genome size reduction have been determined in both groups. One potential explanation is that the cell surface/volume ratio is increased upon reduction in cell size, which enhances nutrient uptake 13. Thi...

Impact of Genome Reduction in Microsporidia

“…Organisms operating under strong reductive selection frequently minimize genomes by eliminating redundancies (Luo et al 2011). In highly reduced picoplanktonic eukaryotic organisms, for example, the total number of gene families is conserved despite extensive gene loss (Derilus et al 2020). Instead, the average size of each gene family is decreased as a result of deletions of paralogous genes.…”

Chromosome-scale assembly of the streamlined picoeukaryote Picochlorum sp. SENEW3 genome reveals Rabl-like chromatin structure and potential for C4 photosynthesis

“…However, unlike other PPEs, such as Ostreococcus, P. SENEW3 displays robust growth in variable environmental conditions, tolerating both euryhaline conditions and temperatures between 16-32 °C [26]. In such extreme or challenging environments, this pressure for adaptive gene loss should be reduced since there are typically fewer community members to produced expensive metabolites [116][117][118]. Hence, the large range of environmental tolerances of P. SENEW3 and payoffs between growth, nutrient availability, and stress, presents an alternate environmental adaptation paradigm for PPEs.…”

“…One hypothesis explaining this genome reduction in PPEs is the Black Queen hypothesis (BQH), which predicts that an availability of shared metabolites in marine environments would drive the loss of redundant metabolic pathways in individual genomes/species that are otherwise available within the surrounding microbial community. Providing a selective advantage by conserving an organism's finite resources through adaptive gene loss [116][117][118]. However, unlike other PPEs, such as Ostreococcus, P. SENEW3 displays robust growth in variable environmental conditions, tolerating both euryhaline conditions and temperatures between 16-32 °C [26].…”

Interaction range of common goods shapes Black Queen dynamics beyond the cheater-cooperator narrative

“…The above cheater-cooperator prediction is sensible for systems with a single common good (Cairns and Jalasvuori, 2018;Cordero et al, 2012;D'Souza et al, 2014;de Mazancourt and Schwartz, 2010;Estrela et al, 2016;Germerodt et al, 2016;Lee et al, 2012;Morris et al, 2012;Ndhlovu et al, 2021;Pande et al, 2016Pande et al, , 2014Shou et al, 2007;Stump et al, 2018;Van Vliet et al, 2022;Wang et al, 2019), and the prediction has been successfully applied to advance our understanding of microbial ecology and evolution (Brunet and Doolittle, 2018;Cairns and Jalasvuori, 2018;D'Souza et al, 2014;Derilus et al, 2020;Hesse and O'brien, 2024;Mas et al, 2016;Morris, 2015b;Morris et al, 2014;Ndhlovu et al, 2021;Takeuchi et al, 2024;Yuan and Meng, 2020). However, most communities in nature are likely to contain more than one common good (Morris, 2015a).…”