Lateral bays of the lower Columbia River estuary are areas of enhanced water retention that influence net ecosystem metabolism through activities of their diverse microbial communities. Metagenomic characterization of sediment microbiota from three disparate sites in two brackish lateral bays (Baker and Youngs) produced ∼100 Gbp of DNA sequence data analyzed subsequently for predicted SSU rRNA and peptide-coding genes. The metagenomes were dominated by Bacteria. A large component of Eukaryota was present in Youngs Bay samples, i.e., the inner bay sediment was enriched with the invasive New Zealand mudsnail, Potamopyrgus antipodarum, known for high ammonia production. The metagenome was also highly enriched with an archaeal ammonia oxidizer closely related to Nitrosoarchaeum limnia. Combined analysis of sequences and continuous, high-resolution time series of biogeochemical data from fixed and mobile platforms revealed the importance of large-scale reciprocal particle exchanges between the mainstem estuarine water column and lateral bay sediments. Deposition of marine diatom particles in sediments near Youngs Bay mouth was associated with a dramatic enrichment of Bacteroidetes (58% of total Bacteria) and corresponding genes involved in phytoplankton polysaccharide degradation. The Baker Bay sediment metagenome contained abundant Archaea, including diverse methanogens, as well as functional genes for methylotrophy and taxonomic markers for syntrophic bacteria, suggesting that active methane cycling occurs at this location. Our previous work showed enrichments of similar anaerobic taxa in particulate matter of the mainstem estuarine water column. In total, our results identify the lateral bays as both sources and sinks of biogenic particles significantly impacting microbial community composition and biogeochemical activities in the estuary.