Metagenomic evidence for reciprocal particle exchange between the mainstem estuary and lateral bay sediments of the lower Columbia River

Abstract

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.

Microbial players and processes involved in phytoplankton bloom utilization in the water column of a fast‐flowing, river‐dominated estuary

“…Once released from dead cells, the 0.5–2 μm chloroplasts can persist in the environment (due to protection afforded by their four membranes; Bedoshvili, Popkova, & Likhoshway, ), and subsequently pass through 3‐μm prefilters collecting on 0.2 μm filters. In prior work, we observed a much higher abundance of diatom chloroplast DNA relative to nuclear DNA in the estuarine water column (Crump, Hopkinson, Sogin, & Hobbie, ) and in unfractionated sediment (Smith et al., ).…”

“…Sequencing of total DNA was done with Hi‐Seq 1000 (Illumina, San Diego, CA). Metagenomes, assembled as described previously (Fortunato & Crump, ; Smith et al., ), were analyzed using the Integrated Microbial Genomes with Microbiome Samples–Expert Review web server (IMG/M‐ER of the DOE Joint Genome Institute, https://img.jgi.doe.gov/cgi-bin/mer/main.cgi; Markowitz et al., ). During this analysis, gene/peptide prediction was done for each assembled contig, and each corresponding gene (including rDNA and predicted peptide coding sequences) was treated as a separate entry.…”

“…Our prior results indicated that deposition of marine diatom particles in the sediments of a brackish lateral bay (Youngs Bay) in the Columbia River estuary was associated with a dramatic enrichment of Bacteroidetes taxa (~60% of total Bacteria) and corresponding genes involved in phytoplankton degradation (Smith et al., ). Members of this taxon are commonly found to dominate phytoplankton bloom‐associated bacterial communities (Buchan, Lecleir, Gulvik, & Gonzalez, ), and more specifically are involved in the initial degradation of coastal blooms (Teeling et al., ).…”

“…Phytoplankton also bloom in the coastal ocean, and provide a smaller but significant input of organic matter to the estuary, particularly in summer and early fall (Amspoker & McIntire, ; Haertel et al., ; Herfort, et al., ; Roegner, Seaton, & Baptista, ). These coastal blooms develop in response to seasonal upwelling (Kudela et al., ) and are transported into the estuary during periods of low river discharge (Roegner et al., ; Smith et al., ). In August–October, estuarine blooms of the mixotrophic ciliate, Mesodinium spp., constitute the only autochthonous POM source from phytoplankton (Herfort, Peterson, McCue, & Crump, et al., ).…”

“…In August–October, estuarine blooms of the mixotrophic ciliate, Mesodinium spp., constitute the only autochthonous POM source from phytoplankton (Herfort, Peterson, McCue, & Crump, et al., ). Dead and degrading phytoplankton blooms are utilized by heterotrophic bacteria and transformed into detritus, DOM and POM that may be utilized in the estuary (Gilbert, Needoba, Koch, Barnard, & Baptista, ), transported to the coastal ocean with the river plume (Small et al., ), or deposited and utilized in estuarine sediments (Smith et al., ).…”