Abstract
The fungus-growing ant-microbe symbiosis is an ideal system to study chemistry-based microbial interactions due to the wealth of microbial interactions described, and the lack of information on the molecules involved therein. In this study, we employed a combination of MALDI imaging mass spectrometry (MALDI-IMS) and MS/MS molecular networking to study chemistry-based microbial interactions in this system. MALDI IMS was used to visualize the distribution of antimicrobials at the inhibition zone between bacteria associated to the ant Acromyrmex echinatior and the fungal pathogen Escovopsis sp. MS/MS molecular networking was used for the dereplication of compounds found at the inhibition zones. We identified the antibiotics actinomycins D, X2 and X0β, produced by the bacterium Streptomyces CBR38; and the macrolides elaiophylin, efomycin A and efomycin G, produced by the bacterium Streptomyces CBR53.These metabolites were found at the inhibition zones using MALDI IMS and were identified using MS/MS molecular networking. Additionally, three shearinines D, F, and J produced by the fungal pathogen Escovopsis TZ49 were detected. This is the first report of elaiophylins, actinomycin X0β and shearinines in the fungus-growing ant symbiotic system. These results suggest a secondary prophylactic use of these antibiotics by A. echinatior because of their permanent production by the bacteria.
Highlights
Symbioses are associations between different organisms which involve a high degree of dependence and coexistence and are broadly distributed in nature[1]
Bacterial strains CBR53 and CBR38 isolated from the propleura of A. echinatior were both identified as Streptomyces sp. based on the analysis of their partial 16S rRNA gene sequences. 16S rRNA gene sequences were deposited in Gene Bank with accession numbers KM096868 and KM096867 for CBR53 and CBR38, respectively
Fungal pathogen strains ACRO424 and TZ49 were identified as Escovopsis sp. based on the partial sequence of the internal transcribed spacers (ITS), sequences were deposited in Gene Bank under the accession numbers KM096865 and KM096866
Summary
Symbioses are associations between different organisms which involve a high degree of dependence and coexistence and are broadly distributed in nature[1] Such associations can be found in any ecosystem including most habitat types on earth, and the effects that one or more members of a symbiotic relationship have on each other can affect the system as a whole[2,3,4,5]. Interactions among antibiotic-producing bacteria (genus Pseudonocardia and Streptomyces) and the mutualistic basidiomycete and Escovopsis have been the subject of several studies Such studies have shown that some ant-associated bacteria are able to produce compounds that inhibit the growth of Escovopsis and other entomopathogens, with and without affecting the cultivar[28,29,30,31]. The few natural products that have been elucidated so far for the system include: dentigerumycin[24]; five angucycline antibiotics (pseudonocardones A–C, 6-deoxy-8-O-methylrabelomycin and X-14881 E)[23], the antifungals (candicidin D, actinomycins D and X, valinomycin, antimycin A1-A4 and a several nystatin-like metabolites)[26, 32,33,34]; two antimycin antibiotics (urauchimycins A and B)[23, 35] (Table 1)
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