Bacterial Biogeography across the Amazon River-Ocean Continuum

Abstract

Spatial and temporal patterns in microbial biodiversity across the Amazon river-ocean continuum were investigated along ∼675 km of the lower Amazon River mainstem, in the Tapajós River tributary, and in the plume and coastal ocean during low and high river discharge using amplicon sequencing of 16S rRNA genes in whole water and size-fractionated samples (0.2-2.0 μm and >2.0 μm). River communities varied among tributaries, but mainstem communities were spatially homogeneous and tracked seasonal changes in river discharge and co-varying factors. Co-occurrence network analysis identified strongly interconnected river assemblages during high (May) and low (December) discharge periods, and weakly interconnected transitional assemblages in September, suggesting that this system supports two seasonal microbial communities linked to river discharge. In contrast, plume communities showed little seasonal differences and instead varied spatially tracking salinity. However, salinity explained only a small fraction of community variability, and plume communities in blooms of diatom-diazotroph assemblages were strikingly different than those in other high salinity plume samples. This suggests that while salinity physically structures plumes through buoyancy and mixing, the composition of plume-specific communities is controlled by other factors including nutrients, phytoplankton community composition, and dissolved organic matter chemistry. Co-occurrence networks identified interconnected assemblages associated with the highly productive low salinity near-shore region, diatom-diazotroph blooms, and the plume edge region, and weakly interconnected assemblages in high salinity regions. This suggests that the plume supports a transitional community influenced by immigration of ocean bacteria from the plume edge, and by species sorting as these communities adapt to local environmental conditions. Few studies have explored patterns of microbial diversity in tropical rivers and coastal oceans. Comparison of Amazon continuum microbial communities to those from temperate and arctic systems suggest that river discharge and salinity are master variables structuring a range of environmental conditions that control bacterial communities across the river-ocean continuum.

Keywords: Amazon River; Columbia River; diatom-diazotroph assemblage; freshwater bacteria; marine bacteria; microbial diversity; river plume; tropical Atlantic Ocean.

FIGURE 1

Map of sampling stations from cruises in the Amazon River plume aboard the R/V Knorr in May/June 2010 (A), and the R/V Melville in September 2011 (B). Amazon River sampling stations from September 2010, December 2010, and May 2011 are indicated on both maps. Surface water salinity along cruise tracks are indicated with colors.

FIGURE 2

Multidimensional Scaling (MDS) diagrams showing Bray–Curtis similarity among bacterial communities in (A) all samples collected in the Amazon River and Plume in 2010 and 2011, (B) Amazon plume samples, and (C) Amazon River samples. Closed symbols represent unfractionated samples and free-living bacteria (0.2–2.0 μm). Open symbols represent particle-attached bacteria (>2.0 μm).

FIGURE 3

Taxonomic diversity and salinity of Amazon River and Plume samples grouped by environment following Figure 2, and showing the most abundant taxonomic groups. River samples are ordered by month in the mainstem river (Óbidos and Macapá), and tributary stations (Belém and Tapajós). Plume samples are ordered by environmental group for the 0.2–2.0 μm and whole water samples, followed by the >2.0 μm fraction samples.

FIGURE 4

The number of positive (blue) and negative (red) edges (i.e., correlations) for indicator taxa within co-occurrence networks for (A) all river samples, and (B) unfractionated and 0.2–2.0 μm plume samples. Line thickness and numbers indicate the number of edges between node groups. Nodes and edges associated with non-indicator taxa are not shown.

FIGURE 5

(A) Multidimensional Scaling (MDS) diagram of Bray–Curtis similarity among bacterial communities in all samples collected for this study, communities from the Columbia River, estuary, plume, and surface ocean (Fortunato et al., 2013), and communities from six arctic rivers (Crump et al., 2009). (B) Average taxonomic diversity of bacterial communities in river, plume, and coastal ocean environments.