Genotype-phenotype modeling of light ecotypes in Prochlorococcusreveals genomic signatures of ecotypic divergence

Abstract

Prochlorococcus species are the most abundant marine photosynthetic bacteria. Despite broadly shared phenotypic traits and marine habitats, they exhibit remarkable genomic diversity. We ask what genomic signatures underlie its ecotypic divergence into high- and low-light adapted lineages, and whether these signatures can still be recovered from incomplete assemblies. From [~]1,000 publicly available Prochlorococcus genomes, we focused on those with information on their light adaptation ecotype (high-light/low-light), phylogenetic clades, and depth of isolation. Across these divisions, we calculated average nucleotide identity and constructed pangenomes to assess cyanobacterial core genes vs. those that separate ecotypes. Despite scant conservation, we observe a sharp taxon separation by light ecotypes. Classical machine learning models trained to predict ecotype achieve near-perfect binary classification accuracy even when predicting on partial genomes (Matthews Correlation Coefficient = 0.86 - 1.00), while regression models trained to predict the depth of isolation performed poorly, with high root mean square error values (37.6 - 42.0m). For ecotype prediction, we analyzed top gene features across model runs and classes; these features included photosynthesis-associated genes and pathways, as well as many novel markers of unknown function. When separating ecotypes further by previously described phylogenetic clades, genomic content and composition show even clearer separation among clades, supporting the taxonomic breadth of the Prochlorococcus collective. These results emphasize the genomic specialization underlying ecotypic divergence and support the utility of ML approaches for cyanobacterial ecotype prediction from metagenomic data. Expanded sampling will yield novel clade-specific biology. All data, models, and results are available on GitHub: https://github.com/JRaviLab/cyano_adaptation. ImportanceProchlorococcus are common aquatic cyanobacteria that can derive energy from light. They can be classified into high-/low-light ecotypes depending on how they use light. Prochlorococcus have small genomes compared to other bacteria, but the gene sets they carry are also remarkably flexible, which may help them survive and adapt to their harsh oceanic environment. We studied hundreds of Prochlorococcus genomes from around the world in an effort to predict ecotypes from partial genome sequences. We used comparative genomics, machine learning, and other statistical methods to identify genomic features associated with ecotypes. These statistical approaches predicted ecotypes accurately, reliably, and according to large differences in gene content and genome structure. Our results support that Prochlorococcus can be divided into different species or genera based on clades, and provide many gene targets for further research to understand cyanobacterial circadian rhythms or improve their bioengineering potential as chassis organisms.