Root bacteriome of a pioneer grass Miscanthus condensatus along restored vegetation on recent Miyake-jima volcanic deposits

Abstract

Root-associated microorganisms play an important role in colonization and subsequent development of pioneer plants on newly exposed substrates such as volcanic deposits. However, there is still lack of an understanding how the root microbiome establishes during a short-term development without apparent soil formation when the pioneer plant colonizes on the pristine substrates. Miscanthus condensatus, the first grass to colonize recent volcanic deposits on the Island of Miyake (Miyake-jima), Japan, is a model plant suitable to address this issue. In this study, we carried out bacterial 16S rRNA gene-based real-time quantitative PCR, T-RFLP profiling and clone library analyses to assess the root bacteriome of M. condensatus from two phases of different plant-colonization, i.e., early colonizing phase (sites OY and IG7) and later dominating phase (sites IG8 and IG9). The results showed that the root-associated bacteriome had comparable 16S rRNA gene densities in the two developmental phases of colonization (4.8–11.7 × 109 and 0.1–0.6 × 109 copies g−1 sample for the rhizosphere and root-endosphere communities, respectively). The rhizosphere community changed significantly between the early and later phases, whereas this change was not as clear for the root-endosphere community. Betaproteobacteria and Gammaproteobacteria respectively occupied 11.7–29.9% and 7.1–14.2% of the rhizosphere community at the early phase and decreased to 4.8–19.1% and 3.5–5.5% of them at the later phase, while the rhizosphere compositions of Alphaproteobacteria and Actinobacteria changed from 14.8 to 16.5% and 8.9–9.0% to 16.8–22.5% and 10.4–18.1 %, respectively. According to the statistic and phylogenetic analyses, the major bacterial genera Paraburkholderia and Trinickia in the class Betaproteobacteria represented the potentially beneficial groups in the root-associated community at the early phase; however, these bacteria were subsequently displaced by the other beneficial bacteria Bradyrhizobium, Rhizobium, Agrobacterium in the class Alphaproteobacteria, and Arthrobacter and Paenarthrobacter in the class Actinobacteria with colonization by this pioneer plant. Our result suggests that bacterial succession occurs in the rhizosphere during the short-term development of pioneer plants on newly exposed volcanic deposits. Such succession partly illustrates how rhizosphere ecosystems become established during colonization and subsequent growth of pioneer plants on newly exposed substrates.