Environmental and anthropogenic controls over bacterial communities in wetland soils

Abstract

Soil bacteria regulate wetland biogeochemical processes, yet little is known about controls over their distribution and abundance. Bacteria in North Carolina swamps and bogs differ greatly from Florida Everglades fens, where communities studied were unexpectedly similar along a nutrient enrichment gradient. Bacterial composition and diversity corresponded strongly with soil pH, land use, and restoration status, but less to nutrient concentrations, and not with wetland type or soil carbon. Surprisingly, wetland restoration decreased bacterial diversity, a response opposite to that in terrestrial ecosystems. Community level patterns were underlain by responses of a few taxa, especially the Acidobacteria and Proteobacteria, suggesting promise for bacterial indicators of restoration and trophic status.

Fig. 1.

Phylogenetic tree of 16S rDNA sequences obtained from freshwater wetland soils derived by parsimony analysis. Percent of total composition of major clades is given from 95 sequences at each of 13 sites. Minor clades are numbered: (1) Nitrospira, 2.6%; (2) unknown, 4.0%; (3) Spirochaetes, 1.3%; (4) Prosectobacter, 2.8%; (5) Planctomycetes, 1.0%. Not shown are Gemmantimonas, 0.7% and Cyanobacteria, 0.7%. Clade sizes are not directly proportionate to percent composition because of uneven inclusion of known guide sequences.

Fig. 2.

Taxonomic composition of bacterial communities across different freshwater wetland ecosystem types and land uses. Taxonomic composition was determined by a phylogenetic tree of 95 clones of bacterial 16S rDNA from each site (Fig. 1). Site abbreviations are color coded by land use: nutrient enriched Everglades sites are brown, agricultural wetlands are red, restored wetlands are blue, and reference wetlands are green. Site abbreviations are described in detail in Materials and Methods.

Fig. 3.

Mantel path analysis linking taxonomic composition of microbial communities to soil chemistry, land use, and wetland type. (A) All wetland types surveyed, land use categories are: Everglades water conservation area (WCA), agriculture, restored, and reference. (B) North Carolina coastal plain wetlands were analyzed separately to determine effects of wetland restoration. Solid lines are partial Mantel correlation coefficients, while dashed lines are pure-partial Mantel correlation coefficients, conditional on all other variables. Where Mantel correlations are significant, line width is proportional to the correlation coefficient, and P values are in parentheses.

Fig. 4.

Soil pH controls bacterial diversity and the relative abundances of select bacterial taxa. Soil pH influences bacterial diversity as assessed by Shannon's index (H') of (A) phylogenetic groups derived from Fig. 1, and (B) species level OTUs, assessed at 97% similarity and derived from Fig. 4. Soil pH also determines the abundance of some bacterial taxa, including (C) Acidobacteria, and (D) Actinobacteria, and α-proteobacteria.

Fig. 5.

Bacterial community ordination by land use, based upon the relative abundance of bacterial taxonomic groups, by principal components analysis. Axis 1 explains 52.6% of variance, while Axis 2 describes an additional 19.2% of variance among samples. Factor loadings are shown with blue vectors for taxonomic groups with >20% loading. Bacterial group abbreviations (clockwise from top) are Acid: Acidobacteria; δ-pr: δ-proteobacteria; GNSB: Green Non Sulfur Bacteria; Nitr: Nitrospira; Spir: Spirochaetes; β-pr: β-proteobacteria; CFB: Cytophaga-Flavobacterium-Bacteriodies; Pros: Prosectobacter; α-pr: α-proteobacteria; Acti: Actinobacteria. Site abbreviations are described in detail in Materials and Methods.

Fig. 6.

Abundance of bacterial taxonomic groups varies with land use across wetland soils. Italicized letters indicate statistical differences determined by Tukey's multiple comparisons. (A) Land use altered the normalized ratio of all Proteobacteria to Acidbacteria with land use (P < 0.001). (B) the abundance of β-proteobacteria was greater in agricultural wetlands than in other land uses (P < 0.001). Statistical grouping of sites was the same for the normalized ratio of β-proteobacteria to Acidobacteria as for the ratio of all Proteobacteria to Acidbacteria (P < 0.001, data in Table S3).

Fig. 7.

Soil bacterial diversity shifts with land use and restoration across NC wetland types. Collector's curves present the number of unique bacterial species (defined at 97%) obtained from a given site, called OTUs. Restoration land use categories are agriculture (red), restored (blue), and reference wetlands (green). Wetland types are (A) pocosin bogs, (B) riverine swamp forests, and (C) nonriverine swamp forests. Site abbreviations are described in detail in Materials and Methods.