Production of the Quorum‐Sensing Molecules N‐Acylhomoserine Lactones by Endobacteria Associated with Mortierella alpina A‐178

Abstract

Gram‐negative bacteria communicate with one another using N‐acylhomoserine lactones (AHLs) as signaling molecules. This mechanism, known as quorum sensing (QS), is needed to develop pathogenicity, as well as symbiotic interactions with eukaryotic hosts, such as animals and plants. Increasing evidence indicates that certain bacteria, namely endobacteria, also inhabit fungal cells and establish symbiotic relationships with their hosts. However, it has not been clear whether bacterial QS acts in developing the relationships. Here we describe the isolation and identification of N‐heptanoylhomoserine lactone and N‐octanoylhomoserine lactone from the culture broth of the zygomycete fungus Mortierella alpina A‐178. This suggested the presence of endobacteria in the fungus, as was confirmed by PCR, fluorescence in situ hybridization, and transmission electron microscopy. Two major bands obtained by PCR‐denaturing gradient gel electrophoresis showed sequence identity to genes in the β‐proteobacterium Castellaniella defragrans (100 %) and the Gram‐positive bacterium Cryobacterium sp. (99.8 %). The production of AHLs depended on the presence of endobacteria and was induced in response to the increase in the concentration of AHLs, suggesting that the bacterium conducts AHL‐mediated QS in the fungus. This paper is the first to report the production of AHLs by endofungal bacteria and raises the possibility that QS plays roles in the development of fungus–endobacterium symbiosis.

Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi

“…There is, however, increasing evidence that Mortierella species (Mucoromycotina) host endobacteria that are related to CaGg (Sato et al, 2010;Kai et al, 2012;Bonito et al, 2013). These data open a novel interesting scenario: fungal endobacteria might prefer coenocytic hyphae.…”

“…Bacterial endosymbionts are widespread among animals (Wernegreen, 2012;McFall-Ngai et al, 2013) and in particular the ones living in insect tissues have been investigated in depth (Ferrari and Vavre, 2011). In contrast, examples of endobacteria living inside the fungal cells are much more limited (Bianciotto et al, 2003;Partida-Martinez and Hertweck, 2005;Lackner et al, 2009;Naumann et al, 2010;Kai et al, 2012).…”

Frontier studies on highly selective bio-regulators useful for environmentally benign agricultural production

“…We screened the ethyl acetate extracts of the culture broths of many fungi isolated from soil, and found that strain Mortierella alpina A-178 produced compounds capable of activating the reporter gene in A. tumefaciens NTL4. Bioassay-based purification, a spectroscopic analysis, and chemical synthesis revealed that the A-178 strain produced N-heptanoylhomoserine lactone (76) 66) and N-octanoylhomoserine lactone (77) 66) together with the novel AHL, (Z)-N-(4-decenoyl)homoserine lactone (78) (Fig. 5).…”

Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica

“…Endofungal bacteria were previously detected in Glomeromycotan arbuscular mycorrhiza symbioses (Bonfante and Anca, 2009;Naumann et al, 2010), in the ectomycorrhizal fungus Laccaria bicolor (Bertaux et al, 2003(Bertaux et al, , 2005, in the rice pathogenic fungus Rhizopus microsporus (Partida-Martinez and Hertweck, 2005), in hyphae of phylogenetically diverse foliar fungal endophytes (Hoffman and Arnold, 2010), in the soil isolate Mortierella alpina (Kai et al, 2012) and the plant symbiotic Endogone Mucoromycotina fungi (Desirò et al, 2015). Endofungal bacteria, associated with fungi of the genera Piriformospora and Sebacina, belong to two genera of Gram-negative (Rhizobium and Acinetobacter) and two genera of Gram-positive (Paenibacillus and Rhodococcus) bacteria.…”