Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance

Abstract

Soils are immensely diverse microbial habitats with thousands of co-existing bacterial, archaeal, and fungal species. Across broad spatial scales, factors such as pH and soil moisture appear to determine the diversity and structure of soil bacterial communities. Within any one site however, bacterial taxon diversity is high and factors maintaining this diversity are poorly resolved. Candidate factors include organic substrate availability and chemical recalcitrance, and given that they appear to structure bacterial communities at the phylum level, we examine whether these factors might structure bacterial communities at finer levels of taxonomic resolution. Analyzing 16S rRNA gene composition of nucleotide analog-labeled DNA by PhyloChip microarrays, we compare relative growth rates on organic substrates of increasing chemical recalcitrance of >2,200 bacterial taxa across 43 divisions/phyla. Taxa that increase in relative abundance with labile organic substrates (i.e., glycine, sucrose) are numerous (>500), phylogenetically clustered, and occur predominantly in two phyla (Proteobacteria and Actinobacteria) including orders Actinomycetales, Enterobacteriales, Burkholderiales, Rhodocyclales, Alteromonadales, and Pseudomonadales. Taxa increasing in relative abundance with more chemically recalcitrant substrates (i.e., cellulose, lignin, or tannin-protein) are fewer (168) but more phylogenetically dispersed, occurring across eight phyla and including Clostridiales, Sphingomonadalaes, Desulfovibrionales. Just over 6% of detected taxa, including many Burkholderiales increase in relative abundance with both labile and chemically recalcitrant substrates. Estimates of median rRNA copy number per genome of responding taxa demonstrate that these patterns are broadly consistent with bacterial growth strategies. Taken together, these data suggest that changes in availability of intrinsically labile substrates may result in predictable shifts in soil bacterial composition.

Keywords: bacteria; bromo-deoxyuridine; carbon; microarray; rRNA copy number; soil; substrate quality.

Figure 1

Phylogeny of bacterial taxa detected following BrdU incorporation. Phyla are designated by branch colors and selected sub-phyla/classes are annotated. The outer rings display the taxa whose relative abundance increased (green) or decreased (red) significantly (p < 0.05 following BH correction) in response to C substrate addition relative to the BrdU-only controls. Outer rings are arranged from the interior in order of expected substrate recalcitrance (glycine, sucrose, cellulose, lignin, tannin–protein).

Figure 2

Non-metric Multidimensional Scaling (NMDS) projection of a Bray–Curtis distance matrix showing the response of actively replicating bacterial communities to C substrate addition. Substrate incubations are depicted with colors and grouped by dotted lines.

Figure 3

Order-level distributions of bacteria significantly (p < 0.05) enriched in response to substrate addition relative to the BrdU-only control. Numbers of enriched taxa are given under each pie and Nearest Taxon Index (NTI) values are in parentheses. *Denotes NTI value significantly different from the null community distribution (p < 0.05).

Figure 4

Euler diagram showing substrate use range of bacterial taxa significantly enriched in response to substrate addition. Pies display the order level taxonomic composition of bacterial taxa enriched only by single substrates, by labile substrates only, and by both labile and chemically recalcitrant substrates. Only expanded pie wedges are included in the legend, a full color legend can be found as supplementary material (Figure S1 in Supplementary Material).