The core root microbiome of Spartina alterniflora is predominated by sulfur-oxidizing and sulfate-reducing bacteria in Georgia salt marshes, USA

Abstract

Background: Salt marshes are dominated by the smooth cordgrass Spartina alterniflora on the US Atlantic and Gulf of Mexico coastlines. Although soil microorganisms are well known to mediate important biogeochemical cycles in salt marshes, little is known about the role of root microbiomes in supporting the health and productivity of marsh plant hosts. Leveraging in situ gradients in aboveground plant biomass as a natural laboratory, we investigated the relationships between S. alterniflora primary productivity, sediment redox potential, and the physiological ecology of bulk sediment, rhizosphere, and root microbial communities at two Georgia barrier islands over two growing seasons.

Results: A marked decrease in prokaryotic alpha diversity with high abundance and increased phylogenetic dispersion was found in the S. alterniflora root microbiome. Significantly higher rates of enzymatic organic matter decomposition, as well as the relative abundances of putative sulfur (S)-oxidizing, sulfate-reducing, and nitrifying prokaryotes correlated with plant productivity. Moreover, these functional guilds were overrepresented in the S. alterniflora rhizosphere and root core microbiomes. Core microbiome bacteria from the Candidatus Thiodiazotropha genus, with the metabolic potential to couple S oxidation with C and N fixation, were shown to be highly abundant in the root and rhizosphere of S. alterniflora.

Conclusions: The S. alterniflora root microbiome is dominated by highly active and competitive species taking advantage of available carbon substrates in the oxidized root zone. Two microbially mediated mechanisms are proposed to stimulate S. alterniflora primary productivity: (i) enhanced microbial activity replenishes nutrients and terminal electron acceptors in higher biomass stands, and (ii) coupling of chemolithotrophic S oxidation with carbon (C) and nitrogen (N) fixation by root- and rhizosphere-associated prokaryotes detoxifies sulfide in the root zone while potentially transferring fixed C and N to the host plant. Video Abstract.

Keywords: Biogeochemical cycles; Microbiome; Rhizosphere; Root; Salt marsh; Spartina alterniflora; Sulfate reduction; Sulfur oxidation.

Fig. 1

Statistical comparisons by linear regression analysis of average plant biomass and leaf natural ¹⁵N abundance (δ¹⁵N) (a), sediment C:N ratio (b), sediment redox potential (Eh) (c), and leaf temperature (d). Plant biomass was calculated as the average of 10 individuals per sampling point. Each leaf δ¹⁵N, sediment C:N ratio, redox potential, and leaf temperature value represents the average of 3, 1, 3, and 5 replicates, respectively

Fig. 2

Statistical comparisons by linear regression analysis of enzyme activity rates and plant biomass assessed at Skidaway Island (a) (c) (e) and Sapelo Island (b) (d) (f). For each sample, rates were calculated from 8 time point measurements. Plant biomass represents the average of 10 individuals per sampling point

Fig. 3

Diversity and abundance of the S. alterniflora microbiome. Boxplots of the Shannon diversity index (a) and prokaryotic abundance determined by qPCR of SSU rRNA genes (b) per microbiome compartment and S. alterniflora phenotype. Evenness across plant compartments assessed by a cumulative rank-abundance plot (c). Non-metric multidimensional scaling (nMDS) ordination of the Bray-Curtis dissimilarity matrix across all collected samples with colors representing microbiome compartment (d) and S. alterniflora phenotype (e). nMDS stress 0.10

Fig. 4

Relative abundance of putative nitrifiers (a), Fe oxidizers (b), S oxidizers (c), and S/sulfate reducers (d) by microbiome compartment and S. alterniflora phenotype

Fig. 5

Prokaryotic identity and relative abundance of the S. alterniflora rhizosphere and root core microbiome. Phylogenetic characterization was conducted using an approximately maximum-likelihood model of the 72 ASVs comprising the S. alterniflora core rhizosphere and root microbiome. Taxonomic information at the genus level is provided for all ASVs. When the taxonomic assignment was unknown at the genus level, the “Unk” prefix was used before the highest resolution taxonomic level assigned