Integrated proteomics and metabolomics suggests symbiotic metabolism and multimodal regulation in a fungal‐endobacterial system

Abstract

Many plant-associated fungi host endosymbiotic endobacteria with reduced genomes. While endobacteria play important roles in these tri-partite plant-fungal-endobacterial systems, the active physiology of fungal endobacteria has not been characterized extensively by systems biology approaches. Here, we use integrated proteomics and metabolomics to characterize the relationship between the endobacterium Mycoavidus sp. and the root-associated fungus Mortierella elongata. In nitrogen-poor media, M. elongata had decreased growth but hosted a large and growing endobacterial population. The active endobacterium likely extracted malate from the fungal host as the primary carbon substrate for energy production and biosynthesis of phospho-sugars, nucleobases, peptidoglycan and some amino acids. The endobacterium obtained nitrogen by importing a variety of nitrogen-containing compounds. Further, nitrogen limitation significantly perturbed the carbon and nitrogen flows in the fungal metabolic network. M. elongata regulated many pathways by concordant changes on enzyme abundances, post-translational modifications, reactant concentrations and allosteric effectors. Such multimodal regulations may be a general mechanism for metabolic modulation.

Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens

“…For instance, the closely related endosymbiont B. rhizoxinica provides its host R. microsporus bacterially derived toxins that facilitate plant tissue invasion by the fungal host offsetting the physiological cost of hosting endobacteria (Lackner et al ., ). Proteomics analysis of the same cured and uncured isolates of Mortierella (AG77) presented here show that the metabolism of the fungal host and bacterium are independent but closely intertwined (Li et al ., ). Although the types of trade‐offs involved in the Mortierella‐Mycoavidus symbiosis are not fully clear yet, the presence of secondary metabolite gene clusters within the M. cysteinexigens (AG77) genome offers intriguing potential tradeoff.…”

Gigaspora margarita with and without its endobacterium shows adaptive responses to oxidative stress

“…The benefits that the endobacteria provide to the fungal partner remain largely unknown, although recent studies on other fungal-bacterial interactions have given some hints Li et al 2017). In a previous study, we combined next-generation sequencing, molecular biology, and cell physiology analyses to compare G. margarita containing CaGg (B+ line) with a "cured" line of the fungus that lacks CaGg (B-line) obtained under laboratory conditions (Lumini et al 2007).…”

The virome of the arbuscular mycorrhizal fungus Gigaspora margarita reveals the first report of DNA fragments corresponding to replicating non‐retroviral RNA viruses in fungi

“…In one case only it has been demonstrated that they are a biologically active component of the symbiosis: a Glomus ( Rhizophagus ) strain free of the GRF1V‐M virus (a virus related to the Giardia‐like virus described in this work) produced a higher amount of spores and promoted plant growth more efficiently than the fungal line containing the virus (Ikeda et al ., ). Similarly a fungal strain of Mortierella elongata cured from its endobacteria produces higher spore numbers and grows better (Li et al ., ). Nevertheless, virus and endobacterial association with AMF seem to be fairly common in nature, raising the possibility of some ecological advantage difficult to measure in the laboratory experimental conditions, where most of the intra‐ and interspecies competition aspects are not under scrutiny.…”