Transcriptomic dissection of Bradyrhizobium sp. strain ORS285 in symbiosis with Aeschynomene spp. inducing different bacteroid morphotypes with contrasted symbiotic efficiency

Abstract

To circumvent the paucity of nitrogen sources in the soil legume plants establish a symbiotic interaction with nitrogen-fixing soil bacteria called rhizobia. During symbiosis, the plants form root organs called nodules, where bacteria are housed intracellularly and become active nitrogen fixers known as bacteroids. Depending on their host plant, bacteroids can adopt different morphotypes, being either unmodified (U), elongated (E) or spherical (S). E- and S-type bacteroids undergo a terminal differentiation leading to irreversible morphological changes and DNA endoreduplication. Previous studies suggest that differentiated bacteroids display an increased symbiotic efficiency (E > U and S > U). In this study, we used a combination of Aeschynomene species inducing E- or S-type bacteroids in symbiosis with Bradyrhizobium sp. ORS285 to show that S-type bacteroids present a better symbiotic efficiency than E-type bacteroids. We performed a transcriptomic analysis on E- and S-type bacteroids formed by Aeschynomene afraspera and Aeschynomene indica nodules and identified the bacterial functions activated in bacteroids and specific to each bacteroid type. Extending the expression analysis in E- and S-type bacteroids in other Aeschynomene species by qRT-PCR on selected genes from the transcriptome analysis narrowed down the set of bacteroid morphotype-specific genes. Functional analysis of a selected subset of 31 bacteroid-induced or morphotype-specific genes revealed no symbiotic phenotypes in the mutants. This highlights the robustness of the symbiotic program but could also indicate that the bacterial response to the plant environment is partially anticipatory or even maladaptive. Our analysis confirms the correlation between differentiation and efficiency of the bacteroids and provides a framework for the identification of bacterial functions that affect the efficiency of bacteroids.© 2018 Society for Applied Microbiology and John Wiley & Sons Ltd.

From Intracellular Bacteria to Differentiated Bacteroids: Transcriptome and Metabolome Analysis in Aeschynomene Nodules Using the Bradyrhizobium sp. Strain ORS285 bclA Mutant

“…Phosphate is often seen as a limiting factor of nitrogen fixation (24). Indeed, the ORS285 strain shows a high expression of genes involved in phosphate and phosphonate import in wild-type bacteroids (18) as well as in the ΔbclA mutant nodule bacteria (see below). The accumulation of phosphoric acid could be due to an absence of its consumption by the nonfunctional ΔbclA nodules.…”

“…Transcriptome analysis of ORS285 in these two different Aeschynomene host plants with contrasting bacteroid types and efficiency has demonstrated that the transition from free-living bacteria to bacteroids is associated with a massive transcriptome switch involving about 20% of the protein-coding genes. Large gene sets are either up-or downregulated in one or both bacteroid types compared to levels in free-living bacteria (18). However, functional analysis of a selected subset of bacteroid-induced genes revealed no symbiotic defects in the mutants, suggesting the robustness of the bacterial symbiotic program or, alternatively, that some of the transcriptional responses are not related to the symbiotic nitrogen fixation process but simply reflect a response to the plant environment.…”

“…In some host species, such as A. afraspera, differentiation results in elongated bacteroids (E-type bacteroids) with moderate polyploidy, while in other species, e.g., A. indica, bacteroids are large spheres (S-type bacteroids) with high polyploidy. The latter are more efficient than the former (18,19). In early nodule development on both host plants, bacteroids differentiate synchronously and very rapidly.…”

“…bacteroids that have undergone the TBD process. However, the level of bacteroid differentiation and the type of bacteroids are different according to the host, and this correlates with the symbiotic efficiency of the symbiosis (6,18). In some host species, such as A. afraspera, differentiation results in elongated bacteroids (E-type bacteroids) with moderate polyploidy, while in other species, e.g., A. indica, bacteroids are large spheres (S-type bacteroids) with high polyploidy.…”

Spotlight on how microbes influence their host's behavior

“…Indeed, besides articles on animal hosts (Koehler et al, 2018;Murfin et al, 2018;Truitt et al, 2018;Altinli et al, 2019;Rothman et al, 2019;Zhao et al, 2019), this special issue contains a number of research papers devoted to understanding how plants respond to their microbial inhabitants. Among these studies on plant-symbiont interactions, several focus on plant responses to nitrogen-fixing bacteria (Lamouche et al, 2018;Baena et al, 2019;Bañuelos-Vazquez et al, 2019;Pujic et al, 2019;Songwattana et al, 2019), while others investigate endophytes and their role in alleviating plant abiotic stress (Vigani et al, 2018;Lanza et al, 2019;Llorens et al, 2019).…”