Controls of SAR11 subclade abundance, diversity, and growth in two Mid-Atlantic estuaries

Abstract

SAR11 is a dominant bacterial clade in marine oligotrophic ecosystems. SAR11 can also be dominant in estuarine systems, where they are not well-studied. We examined the effects of season, nutrient concentrations, and salinity in shaping SAR11 subclade abundance, diversity, function, and growth in two Mid-Atlantic estuaries, the Delaware and Chesapeake Bays. Using metagenome-assembled genomes, we identified twelve distinct genomospecies within the Ia, II, IIIa, and V subclades, which made up to 60% of the total bacterial community. The functional potential of all SAR11 genomospecies varied, especially in carbohydrate metabolism, transporters, and one-carbon metabolic pathways. Predicted growth rates, estimated by the Peak to Trough method, varied by season and genomospecies. SAR11 growth rates negatively correlated in the spring but positively correlated in the summer with chlorophyll a concentrations and bacterial production, as well as phosphate and ammonium concentrations. Genomospecies in Ia.1, IIIa.2, and IIIa.4 subclades had low growth rates, while genomospecies in Ia.3, Ia.5, Ia.6, II, and V subclades had higher and more variable growth rates that were positively correlated with phosphate concentrations and temperature. Growth rate variation between subclades was associated with carbohydrate metabolic gene repertoires, especially glycolysis and number of transporters. While total transcript to genome ratios generally mirrored growth rates, transcription of genes involved in phosphate and nitrogen transport were negatively associated with growth rates. These data suggest that SAR11 genomospecies abundance varies in these estuaries because of differences in growth rates and metabolic capacities in response to changes in environmental conditions. ImportanceThe SAR11 clade is one of the most abundant bacterial groups in marine systems, including many estuaries. From the Delaware Bay and Chesapeake Bay environmental metagenomes, we reconstructed nearly complete SAR11 metagenome-assembled genomes representing ten genomospecies in four subclades, of which at least one is novel. Growth rate estimates of genomospecies correlated with functional gene repertoires of carbohydrate transporter and metabolism. Different SAR11 genomospecies dominated among the seasons, depending on their growth rates, biological productivity, and nutrient concentrations. Our RNAseq approach facilitated an understanding of the environmental controls on the abundance of SAR11 genomospecies in their natural habitat. This study is the first to combine multiple measures of diversity, abundance, functional potential, growth rates and activity of this important group, demonstrating a direct link between SAR11 genomospecies abundance and growth in the context of its environment.