Estimating the maximal growth rates of eukaryotic microbes from cultures and metagenomes via codon usage patterns

Microbial eukaryotes are ubiquitous in the environment and play important roles in key ecosystem processes, including accounting for a significant portion of global primary production. Yet, our tools for assessing the functional capabilities of eukaryotic microbes in the environment are quite limited because many microbes have yet to be grown in culture. Maximum growth rate is a fundamental parameter of microbial lifestyle that reveals important information about an organisms functional role in a community. We developed and validated a genomic estimator of maximum growth rate for eukaryotic microbes, enabling the assessment of growth potential for organisms and communities directly in the environment. We produced a database of over 700 maximum growth rate predictions from genomes, transcriptomes, and metagenome-assembled genomes. By comparing the maximal growth rates of existing culture collections with environmentally-derived genomes we found that, unlike for prokaryotes, culture collections of microbial eukaryotes are only minimally biased in terms of growth potential. We then extended our tool to make community-wide estimates of growth potential from over 500 marine metagenomes, mapping growth potential across the global oceans. We found that prokaryotic and eukaryotic communities have highly correlated growth potentials near the ocean surface, but there is no correlation in their genomic potentials deeper in the water column. This suggests that fast growing eukaryotes and prokaryotes thrive under similar conditions at the ocean surface, but that there is a decoupling of these communities as resources become scarce deeper in the water column.