Resolving the ecological niches of coexisting marine microbial taxa is challenging due to the high species richness of microbial communities and the apparent functional redundancy in bacterial genomes and metagenomes. Here, we generated over 11 million Illumina reads of protein-encoding transcripts collected from well-mixed southeastern US coastal waters to characterize gene expression patterns distinguishing the ecological roles of hundreds of microbial taxa sharing the same environment. The taxa with highest in situ growth rates (based on relative abundance of ribosomal protein transcripts) were typically not the greatest contributors to community transcription, suggesting strong top-down ecological control, and their diverse transcriptomes indicated roles as metabolic generalists. The taxa with low in situ growth rates typically had low diversity transcriptomes dominated by specialized metabolisms. By identifying protein-encoding genes with atypically high expression for their level of conservation, unique functional roles of community members emerged related to substrate use (such as complex carbohydrates, fatty acids, methanesulfonate, taurine, tartrate, ectoine), alternative energy-conservation strategies (proteorhodopsin, AAnP, V-type pyrophosphatases, sulfur oxidation, hydrogen oxidation) and mechanisms for negotiating a heterogeneous environment (flagellar motility, gliding motility, adhesion strategies). On average, the heterotrophic bacterioplankton dedicated 7% of their transcriptomes to obtaining energy by non-heterotrophic means. This deep sequencing of a coastal bacterioplankton transcriptome provides the most highly resolved view of bacterioplankton niche dimensions yet available, uncovering a spectrum of unrecognized ecological strategies.

A PCR approach was used to construct a database of nasA genes (called narB genes in cyanobacteria) and to detect the genetic potential for heterotrophic bacterial nitrate utilization in marine environments. A nasA-specific PCR primer set that could be used to selectively amplify the nasA gene from heterotrophic bacteria was designed. Using seawater DNA extracts obtained from microbial communities in the South Atlantic Bight, the Barents Sea, and the North Pacific Gyre, we PCR amplified and sequenced nasA genes. Our results indicate that several groups of heterotrophic bacterial nasA genes are common and widely distributed in oceanic environments.

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