Rhizosphere heterogeneity shapes abundance and activity of sulfur-oxidizing bacteria in vegetated salt marsh sediments

Abstract

Salt marshes are highly productive ecosystems hosting an intense sulfur (S) cycle, yet little is known about S-oxidizing microorganisms in these ecosystems. Here, we studied the diversity and transcriptional activity of S-oxidizers in salt marsh sediments colonized by the plant Spartina alterniflora, and assessed variations with sediment depth and small-scale compartments within the rhizosphere. We combined next-generation amplicon sequencing of 16S rDNA and rRNA libraries with phylogenetic analyses of marker genes for two S-oxidation pathways (soxB and rdsrAB). Gene and transcript numbers of soxB and rdsrAB phylotypes were quantified simultaneously, using newly designed (RT)-qPCR assays. We identified a diverse assemblage of S-oxidizers, with Chromatiales and Thiotrichales being dominant. The detection of transcripts from S-oxidizers was mostly confined to the upper 5 cm sediments, following the expected distribution of root biomass. A common pool of species dominated by Gammaproteobacteria transcribed S-oxidation genes across roots, rhizosphere, and surrounding sediment compartments, with rdsrAB transcripts prevailing over soxB. However, the root environment fine-tuned the abundance and transcriptional activity of the S-oxidizing community. In particular, the global transcription of soxB was higher on the roots compared to mix and rhizosphere samples. Furthermore, the contribution of Epsilonproteobacteria-related S-oxidizers tended to increase on Spartina roots compared to surrounding sediments. These data shed light on the under-studied oxidative part of the sulfur cycle in salt marsh sediments and indicate small-scale heterogeneities are important factors shaping abundance and potential activity of S-oxidizers in the rhizosphere.

Global-scale structure of the eelgrass microbiome

“…Indeed, abundant bacteria that are predicted sulfur oxidizers have been detected in marine sediments attached to seagrass roots (27), and terminal restriction fragment length polymorphism (T-RFLP) community profiling (43) of root surfaces in a single European seagrass bed has suggested similar patterns in Epsilonproteobacteria community dominance (44). This result is also consistent with observations that Spartina cordgrasses in coastal salt marshes are associated with abundant sulfur-oxidizing bacteria (45).…”

Strong associations between plant genotypes and bacterial communities in a natural salt marsh

“…However, we observed greater abundances of Gammaproteobacteria, which are adapted to relatively high oxygen levels (Thomas et al. (), within the short‐form rhizosphere, that cannot be readily explained by temporal differences in root activity between the growth forms nor by differences in abiotic conditions (i.e., we would expect lower numbers of these bacteria in short‐form habitat due to the more saturated soil, as compared to tall form locations).…”

“…Within the rhizosphere, we found significant differences in community composition depending on whether bacteria were collected from the roots of short‐form or tall‐form S. alterniflora (Figure ). Other studies within northeastern US marshes have reported differences in bacteria among growth forms too, including the entire community in bulk soil (Bowen, Crump, Deegan, & Hobbie, ), and sulfur oxidizers in the rhizosphere (Thomas, Giblin, Cardon, & Sievert, ; although they did not explicitly mention growth forms, their Site 1 was located along the creekbank and thus presumably contained tall form plants, and their Site 2 was on the marsh platform so likely would have consisted of short‐form plants). The major taxonomic differences in our analysis were that rhizosphere microbes associated with tall form plants were dominated by bacteria in the Class Deltaproteobacteria, whereas short‐from microbes were predominantly from the Class Gammaproteobacteria (Figure ).…”

“…The major taxonomic differences in our analysis were that rhizosphere microbes associated with tall form plants were dominated by bacteria in the Class Deltaproteobacteria, whereas short‐from microbes were predominantly from the Class Gammaproteobacteria (Figure ). Microbes that are critical to sulfur cycling in marshes are found in both groups, with many sulfate‐reducing bacteria in the Deltaproteobacteria (Bahr et al., ), and the dominant sulfur oxidizers in the Gammaproteobacteria (Thomas et al., ). Differences in abiotic conditions between the locations where the two growth forms predominantly occur have been used to explain the greater stature of tall form plants—for example, due to higher nitrogen levels (Valiela & Teal, ) or better drainage (Mendelssohn, McKee, & Patrick, ) in tall form habitats—and thus could have directly impacted the structure of microbial communities associated with them in our study.…”

“…For example, Thomas et al. () attributed a greater abundance of Alphaproteobacteria sulfur oxidizers in the rhizosphere of tall form plants to lower sulfide availability for microbes, as a result of greater tidal flushing in tall form soil (their creekside Site 1).…”