Comparative ecological analysis of ribosomal RNA gene copy number in heterotrophic soil bacteria

Ribosomal RNA genes are commonly present in many copies in a bacterial genome among a background of primarily single copy genes. The number of rRNA operons in a genome is a phylogenetically distributed trait within the domain Bacteria, though conserved within individual taxonomic groups. The synthesis of ribosomes is the single largest metabolic expenditure of a bacterial cell, and ribosomal RNA gene copy number imposes a limit on the rate of ribosome biosynthesis. A comparative approach was used in this dissertation to investigate the ecological implications of rRNA gene copy number in heterotrophic soil microbial communities. Bacteria with the same number of rRNA genes were found in divergent phylogenetic lineages and a correlation between evolutionary ancestry and rRNA gene copy number was apparent between strains, species, genera, and higher taxonomic levels. A correlation between evolutionary ancestry and rRNA gene copy number among distantly related bacteria sharing similar ecological niches indicated that rRNA copy number is influenced by environmental selective pressures. Soil microbial communities provided a model system to investigate the relationship between rRNA gene copy number and bacterial response to increased nutrient availability. rRNA gene copy number correlated with the time required for phylogenetically diverse bacteria to form colonies on solid agar media, indicating phenotypic effects associated with rRNA gene copy number. Soil bacteria that rapidly formed colonies possessed a significantly greater number of rRNA genes per genome than later appearing colonies. The hypothesis was tested that heterotrophic soil bacteria with many rRNA genes possess an increased capacity for rRNA synthesis permitting rapid increases in cellular rRNA content and growth. In soil microcosms amended with succinate, rapid increases in rRNA abundance and growth were observed in phylogenetic groups of bacteria possessing many (≥4) rRNA genes per genome. In contrast, increases in rRNA abundance and growth were not observed in phylogenetic groups of bacteria with few (≤3) rRNA genes following succinate amendment. Bacteria with few rRNA genes per genome comprised the largest fraction of the soil microbial community. An ecological trade-off in growth rate versus numerical growth yield was rejected as an explanation for the high abundance of slow growing bacteria in soil. Maximal growth rates were positively correlated with rRNA gene copy number, however, several bacteria with many rRNA operons were unable to grow at low nutrient concentrations. The research described in this dissertation demonstrates that rRNA gene copy number reflects the metabolic capacity of bacteria for rRNA synthesis and growth, providing a genetic indicator of bacterial ecological strategies for responding to nutrient availability.