Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years

Abstract

Microbial activities that affect global oceanographic and atmospheric processes happen throughout the water column, yet the long-term ecological dynamics of microbes have been studied largely in the euphotic zone and adjacent seasonally mixed depths. We investigated temporal patterns in the community structure of free-living bacteria, by sampling approximately monthly from 5 m, the deep chlorophyll maximum (∼15-40 m), 150, 500 and 890 m, in San Pedro Channel (maximum depth 900 m, hypoxic below ∼500 m), off the coast of Southern California. Community structure and biodiversity (inverse Simpson index) showed seasonal patterns near the surface and bottom of the water column, but not at intermediate depths. Inverse Simpson's index was highest in the winter in surface waters and in the spring at 890 m, and varied interannually at all depths. Biodiversity appeared to be driven partially by exchange of microbes between depths and was highest when communities were changing slowly over time. Meanwhile, communities from the surface through 500 m varied interannually. After accounting for seasonality, several environmental parameters co-varied with community structure at the surface and 890 m, but not at the intermediate depths. Abundant and seasonally variable groups included, at 890 m, Nitrospina, Flavobacteria and Marine Group A. Seasonality at 890 m is likely driven by variability in sinking particles, which originate in surface waters, pass transiently through the middle water column and accumulate on the seafloor where they alter the chemical environment. Seasonal subeuphotic groups are likely those whose ecology is strongly influenced by these particles. This surface-to-bottom, decade-long, study identifies seasonality and interannual variability not only of overall community structure, but also of numerous taxonomic groups and near-species level operational taxonomic units.

Figure 1

Median values of environmental parameters at each depth for each month across the 10-year SPOT data set. Symbols represent depth at which the parameter was measured. Confidence bars are plus or minus one median adjusted deviation.

Figure 2

Mean Bray-Curtis similarities of all pairs of samples (y axis) separated by different intervals of time (x axis). Circles represent the mean similarity of all pairs of samples taken a given number of months apart (intermonthly; left y axis). Thus, the first circle is the mean Bray-Curtis similarity of all pairs of samples taken 15–45 days (∼1 month) apart, the second circle is the mean similarity of all pairs of samples taken 46–76 days (∼2 months), the twelfth circle (aligned with the 1-year lag tick mark) represents samples taken 12 months apart and so on. Squares represent mean similarity of samples taken a given number of years apart (interannual; right y axis). Accordingly, the first square represents the mean Bray-Curtis similarity of all pairs of samples taken less than 1 year apart, the second is all pairs of samples taken between 1 and 2 years apart and so on. Error bars, for both types of data points, represent 95% confidence intervals of the mean similarity. Points with non-overlapping error bars suggest statistically significant differences in mean similarity between samples taken different distances apart in time. For instance, samples taken 6 months apart in the surface (the sixth circular data point) are statistically less similar than samples taken 1 month apart (first circular point), while samples taken 12 months apart (twelfth circular point) are not less similar than samples taken 1 month apart.

Figure 3

(a) Mean biodiversity index scores by depth. X axis labels are the biodiversity metrics under evaluation. Richness is mean number of species in a given sample with greater than 1%, 0.1% and 0.01%. Inverse Simpson (ISI) and Shannon H are biodiversity indexes and Pelou J measures evenness. Y axes are the values for each metric (OTUs for richness and inverse Simpson's index, unitless for Shannon Biodiversity and Peilou's evenness. Symbols represent depths and are described in the legend. Bars represent 95% confidence intervals from the mean. (b) Similarity between communities at 150 and 500 m (x axis) compared with the ISI of the community at 150 m (y axis). Each point represents the relationship between ISI and similarity between depths for a single month. The solid line is a trend line and the dashed lines represent 95% confidence intervals of this trend. The R-value of this correlation is 0.49 with associated confidence intervals from 0.30 to 0.64. This R-value and its confidence interval correspond to the darkened symbol and bar in (c). This figure is provided as an example of correlations seen between depths and ISI shown in (c). Other pairs of depths, shown in (c), show similar trends. (c) R-values of correlations (y axis) between inverse Simpson index (ISI) values for each depth given as a symbol, and its similarity to other depths or to the previous month (x axis). Symbol shapes signify depth at which the biodiversity was measured. The first five parameters signify the Bray-Curtis similarity between that the depth measured (indicated by symbol) and each other depth (vs5m, vsDCM, vs150m, vs500m, vs890m). Higher R-values represent a stronger correlation between the biodiversity at the measured depth and its similarity to the depth given by the x label. For instance, the y value of the darkened diamond shape is 0.32, corresponding to slope of the relationship between biodiversity at 150 m and interdepth similarity between 150 m and 500 m depicted in (b). The ‘vsLastMonth' column represents the relationship between ISI and the Bray-Curtis similarity between that sample and a sample taken at that same depth collected in the previous month. Bars represent 95% confidence intervals for the R-value. Confidence intervals not overlapping the x axis indicate statistically significant correlations.

Figure 4

Heat map of relative abundances of bacteria from class and phylum level taxonomic groups (a) as well as family and order level groups (b). Each panel represents a different taxonomic grouping. The x axis indicates months and y axis indicates sampled depths (not to scale). Colors correspond to the summed relative abundance of all OTUs identified as falling within that taxonomic group, averaged by month. Relative abundance scores for each color are given in the scale bar at right; note that abundances are on a log scale.