Diversity, composition, and geographical distribution of microbial communities in California salt marsh sediments

Abstract

The Pacific Estuarine Ecosystem Indicators Research Consortium seeks to develop bioindicators of toxicant-induced stress and bioavailability for wetland biota. Within this framework, the effects of environmental and pollutant variables on microbial communities were studied at different spatial scales over a 2-year period. Six salt marshes along the California coastline were characterized using phospholipid fatty acid (PLFA) analysis and terminal restriction fragment length polymorphism (TRFLP) analysis. Additionally, 27 metals, six currently used pesticides, total polychlorinated biphenyls and polycyclic aromatic hydrocarbons, chlordanes, nonachlors, dichlorodiphenyldichloroethane, and dichlorodiphenyldichloroethylene were analyzed. Sampling was performed over large (between salt marshes), medium (stations within a marsh), and small (different channel depths) spatial scales. Regression and ordination analysis suggested that the spatial variation in microbial communities exceeded the variation attributable to pollutants. PLFA analysis and TRFLP canonical correspondence analysis (CCA) explained 74 and 43% of the variation, respectively, and both methods attributed 34% of the variation to tidal cycles, marsh, year, and latitude. After accounting for spatial variation using partial CCA, we found that metals had a greater effect on microbial community composition than organic pollutants had. Organic carbon and nitrogen contents were positively correlated with PLFA biomass, whereas total metal concentrations were positively correlated with biomass and diversity. Higher concentrations of heavy metals were negatively correlated with branched PLFAs and positively correlated with methyl- and cyclo-substituted PLFAs. The strong relationships observed between pollutant concentrations and some of the microbial indicators indicated the potential for using microbial community analyses in assessments of the ecosystem health of salt marshes.

FIG. 1.

Samples were collected from six salt marshes along the California coast, four in the north (A) and two in the south (B). Samples were collected along the channel (C) and at different depths (D). Table 1 shows the numbers of samples collected.

FIG. 2.

Correlation of total biomass (PLFA) with organic carbon and total nitrogen contents in sediments.

FIG. 3.

Ordination plots of CA results, showing variation between 2002 samples (•) and 2003 samples (○) in PLFA and TRFLP fingerprints.

FIG. 4.

Ordination plots of CA of PLFA (A) and TRFLP (B) fingerprints by marsh and correlation of CA scores to latitude (C). Only samples collected in 2003 were included. The data are means ± standard errors; the numbers of samples are shown in Table 1.

FIG. 5.

Ordination plots of CCA results for PLFA (A) and TRFLP (B) fingerprints. Only variables describing spatial variation (marsh, elevation) and sampling year were included in this analysis. The direction of an arrow indicates the steepest increase in the variable, and the length indicates the strength relative to other variables.

FIG. 6.

(A and B) Total PLFA biomass at different elevations for sites sampled in 2002 (A) and 2003 (B). (C and D) PLFA biomarker ratios for monounsaturated and saturated fatty acids (C) and 18:2ω6c,9c and bacteria (D) in 2003. Different letters above bars for the same marsh indicate that the values are significantly different at a level of P = 0.05.

FIG. 7.

Sample ordination plots of CCA results for PLFA (A) and TRFLP (B) fingerprints. The analysis included all variables, before pCCA. Polygons indicate sample groups.

FIG. 8.

Ordination plots of pCCA results for PLFA fingerprints. Elevation, latitude, and year were used as covariables. The arrows represent the best 10 variables by automatic forward selection in CANOCO. Fatty acid groups (branched, saturated, cyclo, etc.) were included as supplementary variables and are not determinants of the sample ordination. UNSAT, unsaturated fatty acids; MUNSAT, monounsaturated fatty acids; SAT, saturated fatty acids; Eukaryot, eukaryote; SRB, sulfate-reducing bacteria.