Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth

Abstract

Background Despite the knowledge that the soil–plant–microbiome nexus is shaped by interactions amongst its members, very little is known about how individual symbioses regulate this shaping. Even less is known about how the agriculturally important symbiosis of nitrogen-fixing rhizobia with legumes is impacted according to soil type, yet this knowledge is crucial if we are to harness or improve it. We asked how the plant, soil and microbiome are modulated by symbiosis between the model legume Medicago truncatula and different strains of Sinorhizobium meliloti or Sinorhizobium medicae whose nitrogen-fixing efficiency varies, in three distinct soil types that differ in nutrient fertility, to examine the role of the soil environment upon the plant–microbe interaction during nodulation. Results The outcome of symbiosis results in installment of a potentially beneficial microbiome that leads to increased nutrient uptake that is not simply proportional to soil nutrient abundance. A number of soil edaphic factors including Zn and Mo, and not just the classical N/P/K nutrients, group with microbial community changes, and alterations in the microbiome can be seen across different soil fertility types. Root endosphere emerged as the plant microhabitat more affected by this rhizobial efficiency-driven community reshaping, manifested by the accumulation of members of the phylum Actinobacteria. The plant in turn plays an active role in regulating its root community, including sanctioning low nitrogen efficiency rhizobial strains, leading to nodule senescence in particular plant–soil–rhizobia strain combinations. Conclusions The microbiome–soil–rhizobial dynamic strongly influences plant nutrient uptake and growth, with the endosphere and rhizosphere shaped differentially according to plant–rhizobial interactions with strains that vary in nitrogen-fixing efficiency levels. These results open up the possibility to select inoculation partners best suited for plant, soil type and microbial community.

Ammonia leakage can underpin nitrogen-sharing among soil microbes

“…The presented findings are relevant in our understanding of nitrogen dynamics in soils. Nitrate is a major component of global soils ([Hill et al, 2011], ([Lagunas et al, 2023]), [Craswell, 2021], [Walvoord et al, 2003], [Rao and Puttanna, 2000]) and applied fertilisers making it an abundant source of nitrogen for many microorganisms and plants. Assimilating nitrate is an energetically expensive process, necessitating both active uptake of nitrate and its reduction to ammonia ([Moreau et al, 2019], [Lin and Stewart, 1997], [Crawford and Arst Jr, 1993]).…”

“…In addition to its inability to produce thiamine, S. indica has been shown previously to have impaired growth in media with nitrate as the only N-source, and lacks genes coding for nitrate transporters and, nitrate and nitrite reductases ([Zuccaro et al, 2011]). Considering that nitrate is a major nitrogen source in global soils and agricultural practices ([Hill et al, 2011], [Lagunas et al, 2023], [Craswell, 2021], [Walvoord et al, 2003], [Rao and Puttanna, 2000]), this raises a question about why fungi such as S. indica would lose there ability to assimilate such an abundant nitrogen source and how they sustain themselves in nitrate-dominant environments. One possible answer to these questions could be that alternative nitrogen sources that are easier to utilise to be readily co-existing with nitrate, in nitrate-rich environments due to activities of nitrate utilising bacteria.…”

What happens with bacteria in the roots affects what happens with fungi in the leaves

“…In addition, plants of the Fabaceae family can recruit different types of soil microorganisms according to their ability to form nodules or not (Chang et al, 2017; Lagunas et al, 2023); thus, not only particular groups of nitrogen-fixing bacteria are associated with certain legume species, but the presence of a nitrogen-fixing symbiosis is directly involved in the selection of specific microbial taxa and changes in the host community (Lagunas et al, 2023; Mahmud et al, 2020; Trivedi et al, 2020; Zgadzaj et al, 2016).…”

“…Several chemical compounds, secondary metabolites, mucilage, and nutrients present in the root exudate can act as a selective force, attracting and favoring specific microorganisms. These selected microorganisms then migrate from the root to different plant organs, with the leaves being the main destination (Chaparro et al, 2014; Ferguson et al, 2019; Lagunas et al, 2023; Sánchez-Cañizares et al, 2017).…”

“…This study reveals that interactions of Fabaceae plants with nitrogen-fixing bacteria in roots have a substantial impact on the richness and diversity of the mycobiome present in leaves. This finding suggests that dynamics at the root level can significantly influence the composition of fungal communities in other plant tissues (Lagunas et al, 2023;Mahmud et al, 2020). The lack of research addressing the influence of specific fungal orders in determining diversity based on nodulation capacity highlights the need for further exploration of these orders and their relationship to the establishment of plant-microorganism symbiosis.…”