Mangrove-diazotroph relationships at the root, tree and forest scales: diazotrophic communities create high soil nitrogenase activities in Rhizophora stylosa rhizospheres

Abstract

Background and aims: The tidal flats on which mangrove plants grow tend to have low soil nitrogen contents because nitrogen-containing litter is repeatedly washed offshore by ebb tides. Under such circumstances, it is unclear how mangrove plants acquire the nitrogen required to support their vigorous growth. In the present work, chemical and biological characteristics of diazotrophy around mangrove plant roots were surveyed under natural conditions to elucidate mangrove-diazotroph relationships.

Methods: Soil nitrogenase activity of a representative mangrove plant, Rhizophora stylosa, which has a broad geographical distribution, was measured using the acetylene reduction assay at forest, tree and prop root scales. In addition, diazotrophic community composition was compared between rhizosphere and bulk soil based on sequencing of nifH genes.

Key results: Soil nitrogenase activity was high near prop roots, and this pattern was enhanced as soil live root content increased. At the forest scale, we observed high soil nitrogenase activity (acetylene-reducing activity) inside the forest (the highest value was 90.9 µmol C2H2 min-1 cm-3, average 46.8 ± 18.2 µmol C2H2 min-1 cm-3). Rates decreased sharply from the forest to the tidal flat (range 1.2-22.2 µmol C2H2 min-1 cm-3, average 7.9 ± 4.5 µmol C2H2 min-1 cm-3). The nifH operational taxonomic unit composition differed significantly among forest and tree rhizospheres and the bulk soil (P < 0.0001).

Conclusions: Our results suggest that the accumulation of diazotrophs around R. stylosa mangrove trees enhances the supply of biologically fixed nitrogen to the mangrove roots. This supply is especially important when the soil naturally contains little nitrogen. This nitrogen acquisition system may be a key process that explains the high productivity of mangrove ecosystems.

Keywords: Rhizophora stylosa; ARA; Diazotrophs; biological nitrogen fixation; mangroves; nitrogen; nitrogenase.