Our view of genome size in Archaea and Bacteria has remained skewed as the data has been dominated by genomes of microorganisms that have been cultivated under laboratory settings. However, the continuous effort to catalog Earth’s microbiomes, specifically propelled by recent extensive work on uncultivated microorganisms, provides an opportunity to revise our perspective on genome size distribution. We present a meta-analysis that includes 26,101 representative genomes from 3 published genomic databases; metagenomic assembled genomes (MAGs) from GEMs and stratfreshDB, and isolates from GTDB. Aquatic and host-associated microbial genomes present on average the smallest estimated genome sizes (3.1 and 3.0 Mbp, respectively). These are followed by terrestrial microbial genomes (average 3.7 Mbp), and genomes from isolated microorganisms (average 4.3 Mbp). On the one hand, aquatic and host-associated ecosystems present smaller genomes sizes in genera of phyla with genome sizes above 3 Mbp. On the other hand, estimated genome size in phyla with genomes under 3 Mbp showed no difference between ecosystems. Moreover, we observed that when using 95% average nucleotide identity (ANI) as an estimator for genetic units, only 3% of MAGs cluster together with genomes from isolated microorganisms. Although there are potential methodological limitations when assembling and binning MAGs, we found that in genome clusters containing both environmental MAGs and isolate genomes, MAGs were estimated only an average 3.7% smaller than isolate genomes. Even when assembly and binning methods introduce biases, estimated genome size of MAGs and isolates are very similar. Finally, to better understand the ecological drivers of genome size, we discuss on the known and the overlooked factors that influence genome size in different ecosystems, phylogenetic groups, and trophic strategies.

Background Microorganisms in the seafloor use a wide range of metabolic processes, which are coupled to the presence of functional genes within their genomes. Aquatic environments are heterogenous and often characterized by natural physiochemical gradients that structure these microbial communities potentially changing the diversity of functional genes and its associated metabolic processes. In this study, we investigated spatial variability and how environmental variables structure the diversity and composition of benthic functional genes and metabolic pathways across various fundamental environmental gradients. We analyzed metagenomic data from sediment samples, measured related abiotic data (e.g., salinity, oxygen and carbon content), covering 59 stations spanning 1,145 km across the Baltic Sea. Results The composition of genes and microbial communities were mainly structured by salinity plus oxygen, and the carbon to nitrogen (C:N) ratio for specific metabolic pathways related to nutrient transport and carbon metabolism. Multivariate analyses indicated that the compositional change in functional genes was more prominent across environmental gradients compared to changes in microbial taxonomy even at genus level, and indicate functional diversity adaptation to local environments. Oxygen deficient areas (i.e., dead zones) were more different in gene composition when compared to oxic sediments. Conclusions This study highlights how benthic functional genes are structured over spatial distances and by environmental gradients and resource availability, and suggests that changes in, e.g., oxygenation, salinity, and carbon plus nitrogen content will influence functional metabolic pathways in benthic habitats.

Our view of genome size distribution in Bacteria and Archaea has remained skewed as the data used to paint its picture has been dominated by genomes of microorganisms that can be cultivated under laboratory settings. However, the continuous effort to catalogue the genetic make-up of Earth’s microbiomes, specifically propelled by recent extensive work on uncultivated microorganisms, provides a unique opportunity to revise our perspective on genome size distribution. Genome size is largely a function of the expansion and contraction, by gain or loss of DNA elements. While genome expansion provides microorganisms the capability to acquire a wide repertoire of ecological functions, genome reduction increases the fitness of the microorganisms to very specific niches. Capitalizing on a recently released large catalog of tens of thousands of metagenome-assembled genomes, we here provide a comprehensive overview of genome size distributions, suggesting that the known phylogenetic diversity of environmental microorganisms possess significantly smaller genomes (aquatic bacteria average 3.1 Mb, host-associated bacterial genomes average 3.0 Mb, and terrestrial bacteria average 3.8 Mb) than the collection of laboratory isolated microorganisms (average 4.4 Mb). Moreover, the variation in genome sizes across different types of environments reflects the different ecological and evolutionary strategies used by microorganisms to thrive in their native environment. Finally, the fact that genome sizes in Bacteria and Archaea remain relatively small might be a reflection of the constraints imposed by selection and an overall dominance of gene loss as a survival strategy.