A genomic perspective across Earth’s microbiomes reveals that genome size in Archaea and Bacteria is linked to ecosystem type and trophic strategy

Abstract

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.

Candidatus Methylumidiphilus Drives Peaks in Methanotrophic Relative Abundance in Stratified Lakes and Ponds Across Northern Landscapes

“…Methylumidiphilus alinensis, GCA_003242955.1). In comparison, the average for environmental aquatic bacteria is 3.1 Mb (Rodríguez-Gijón et al, 2021). However, the observed high level of dominance seems unlikely to only be due to a methodological bias.…”

A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH

“…Given the observation that genome size is negatively correlated with pH in acidophiles, we aimed to determine what genomic processes influence this relationship. Figure 5A shows a diagrammatic representation of genetic mechanisms that have been postulated to be involved in genome expansion or reduction in Bacteria and Archaea ( Keeling and Slamovits, 2005 ; Sabath et al, 2013 ; Giovannoni et al, 2014 ; Gillings, 2017 ; Kirchberger et al, 2020 ; Rodríguez-Gijón et al, 2021 ; Westoby et al, 2021 ). Genome size changes could result from having changes in the number of orthologous families (i, Figure 5A ) or paralogous genes (ii, Figure 5A ), in genome compaction/expansion resulting from changes in the number of intergenic nucleotides, including alteration in the frequency of overlapping genes (iii, Figure 5A ; reviewed in Kirchberger et al, 2020 ), and in smaller or larger genes, including loss/gain of domains (iv, Figure 5A ).…”

“…Significant differences in genome sizes (number of base pairs per genome) have been detected between closely related lineages of prokaryotes isolated from a broad spectrum of environments, with genome sizes down to 1.2 Mbp in free-living bacteria ( Konstantinidis and Tiedje, 2004 ; Dufresne et al, 2005 ; Lynch, 2006 ; Giovannoni et al, 2014 ; Bentkowski et al, 2015 ; Martínez-Cano et al, 2015 ; Rodríguez-Gijón et al, 2021 ). Small or reduced genomes, also termed streamlined genomes, have been widely observed in microorganisms adapted to live in low-nutrient niches, such as cosmopolitan marine bacterioplankton ( Giovannoni et al, 2005 ; Schneiker et al, 2006 ; Swan et al, 2013 ; Luo et al, 2014 ; Sun and Blanchard, 2014 ; Graham and Tully, 2021 ), rivers ( Nakai et al, 2016 ), slow growers in anoxic subsurfaces ( Chivian et al, 2008 ; McMurdie et al, 2009 ), and in a wide range of extremophiles such as bacteria adapted to supersaturated silica ( Saw et al, 2008 ), halophiles ( López-Pérez et al, 2013 ; Min-Juan et al, 2016 ), thermophiles ( Sabath et al, 2013 ; Saha et al, 2015 ; Gu et al, 2021 ), psychrophiles ( Dsouza et al, 2014 ; Goordial et al, 2016 ), and alkaliphiles ( Suzuki et al, 2014 ).…”

Taxonomic and functional diversity of aquatic heterotrophs is sustained by dissolved organic matter chemodiversity

“…Despite the significance of microorganisms as mediators of biogeochemical processes in aquatic environments, their ecological niches in the turnover of the DOM pool are still unresolved. This is at least in part because aquatic microbial diversity is high while many abundant microbes remain uncultivated (Rodríguez-Gijón et al 2022), and also because of the high complexity and dynamic nature of aquatic DOM (Patriarca et al 2020b).…”