Metabolic modelling reveals the specialization of secondary replicons for niche adaptation in Sinorhizobium meliloti

Abstract

The genome of about 10% of bacterial species is divided among two or more large chromosome-sized replicons. The contribution of each replicon to the microbial life cycle (for example, environmental adaptations and/or niche switching) remains unclear. Here we report a genome-scale metabolic model of the legume symbiont Sinorhizobium meliloti that is integrated with carbon utilization data for 1,500 genes with 192 carbon substrates. Growth of S. meliloti is modelled in three ecological niches (bulk soil, rhizosphere and nodule) with a focus on the role of each of its three replicons. We observe clear metabolic differences during growth in the tested ecological niches and an overall reprogramming following niche switching. In silico examination of the inferred fitness of gene deletion mutants suggests that secondary replicons evolved to fulfil a specialized function, particularly host-associated niche adaptation. Thus, genes on secondary replicons might potentially be manipulated to promote or suppress host interactions for biotechnological purposes.

Exploring the evolutionary dynamics of Rhizobium plasmids through bipartite network analysis

“…Further work aimed at identifying the selective forces acting on both symbiotic and accessory plasmids and responsible for variation in nitrogen fixation efficiency should also help in understanding their co-evolutionary framework ruling the evolution of Rhizobium-legume symbiosis (Remigi et al, 2014). Given the increasing availability and utilization of multiomics sequencing with the rapid development of network analysis approaches, such as multipartite network and multilayer network, we can expect to better understand these intriguing genetic elements in various lifestyles of all rhizobial bacteria (diCenzo et al, 2016;Marx et al, 2016).…”

“…NGR234 (also called Sinorhizobium fredii NGR234) undergoes large-scale DNA rearrangements involving replicon fusions and excisions, promoted mainly by homologous recombination between insertion sequence elements (Mavingui et al, 2002). It is proposed that the non-random organization of bacterial genomes is shaped by selective pressures to facilitate host interactions and niche adaptation (diCenzo et al, 2016). However, the evidence to support such a hypothesis in rhizobia is lacking (MacLean and San Millan, 2015).…”

The ModelSEED Database for the integration of metabolic annotations and the reconstruction, comparison, and analysis of metabolic models for plants, fungi, and microbes

“…Beyond the capacity of models to give structure and chemical meaning to functional annotations in biology, these models are also valuable for their predictive capacity. Today, models can be used to predict a wide range of biological phenotypes, including: (i) respiration, photosynthesis, and fermentation types (Cheung et al 2014;de la Torre et al 2015;Marcellin et al 2016;Edirisinghe et al 2016;Meadows et al 2016;Mendoza et al 2017;Marshall et al 2017;Chen et al 2018;Shameer et al 2018;Lieven et al 2018); (ii) feasible growth conditions and Biolog phenotype array profiles (Plata et al 2015;Bosi et al 2016;diCenzo et al 2016;Hartleb et al 2016); (iii) essential genes and reactions (Ding et al 2016;Khodayari and Maranas 2016;Zhang et al 2018;Xavier et al 2018;Guzmán et al 2018); (iv) potential existing or engineerable by-product biosynthesis pathways (Alper et al 2005;Milne et al 2011;Park et al 2013;Chen and Henson 2016;Harder et al 2016); and (v) the yields and even titre available for those pathways (Zuñiga et al 2016;Wang et al 2017;Li et al 2018;Niu et al 2019).…”

A Virtual Nodule Environment (ViNE) for modelling the inter-kingdom metabolic integration during symbiotic nitrogen fixation

“…Despite the importance of metabolism to SNF (18), there has been limited use of metabolic modelling in the study of rhizobia and SNF. To date, GENREs of varying quality have been reported for only three rhizobia: Sinorhizobium meliloti (33–35), Rhizobium etli (36–38), and Bradyrhizobium diazoefficiens (39). Currently, M. truncatula (40) and Glycine max (41) are the only legumes with published GENREs.…”