Abundant antibiotic resistance genes in rhizobiome of the human edible Moringa oleifera medicinal plant

Abstract

Moringa oleifera (or the miracle tree) is a wild plant species widely grown for its seed pods and leaves, and is used in traditional herbal medicine. The metagenomic whole genome shotgun sequencing (mWGS) approach was used to characterize antibiotic resistance genes (ARGs) of the rhizobiomes of this wild plant and surrounding bulk soil microbiomes and to figure out the chance and consequences for highly abundant ARGs, e.g., mtrA, golS, soxR, oleC, novA, kdpE, vanRO, parY, and rbpA, to horizontally transfer to human gut pathogens via mobile genetic elements (MGEs). The results indicated that abundance of these ARGs, except for golS, was higher in rhizosphere of M. oleifera than that in bulk soil microbiome with no signs of emerging new soil ARGs in either soil type. The most highly abundant metabolic processes of the most abundant ARGs were previously detected in members of phyla Actinobacteria, Proteobacteria, Acidobacteria, Chloroflexi, and Firmicutes. These processes refer to three resistance mechanisms namely antibiotic efflux pump, antibiotic target alteration and antibiotic target protection. Antibiotic efflux mechanism included resistance-nodulation-cell division (RND), ATPbinding cassette (ABC), and major facilitator superfamily (MFS) antibiotics pumps as well as the two-component regulatory kdpDE system. Antibiotic target alteration included glycopeptide resistance gene cluster (vanRO), aminocoumarin resistance parY, and aminocoumarin self-resistance parY. While, antibiotic target protection mechanism included RbpA bacterial RNA polymerase (rpoB)-binding protein. The study supports the claim of the Frontiers in Microbiology 01 frontiersin.org Shami et al. 10.3389/fmicb.2022.990169 possible horizontal transfer of these ARGs to human gut and emergence of new multidrug resistant clinical isolates. Thus, careful agricultural practices are required especially for plants used in circles of human nutrition industry or in traditional medicine.

Functional annotation of rhizospheric phageome of the wild plant species Moringa oleifera

“…The presence of non-viral genes in bacteriophages, likely occurring accidentally, is an intermediate step toward the horizontal gene transfer (HGT) and the spreading of one or more genes within a microbiome of a given host (Berglund, 2015 ). Horizontal transfer of bacterial genes via transformation, conjugation, and transduction to their analogs in the human pathogenic strains was speculated to be possible (Andersson and Hughes, 2010 ; Shami et al, 2022 ). The transduction of ARGs among bacteria via bacteriophages was almost neglected although phages are estimated to be the most abundant biological entities on Earth (Dion et al, 2020 ).…”

Functional analysis of bacterial genes accidentally packaged in rhizospheric phageome of the wild plant species Abutilon fruticosum

“…This term refers to the bacteria's low affinity for the antibiotic-binding site ( Munita and Arias, 2016 ). Antibiotic target alteration includes resistance to aminocoumarin and self-resistance parY gene of the genus Streptomyces ( Schmutz et al, 2003 , Schmutz et al, 2004 , Li and Heide, 2006 , Shami et al, 2022 ). Self-resistance refers to antibiotic-producing bacteria that harbor highly complex self-defense mechanisms against their own antibiotics ( Peterson and Kaur, 2018 ).…”

“…Virome, particularly phageome, is a major candidate for such an incidence of HGT if it is accidentally packaged with bacterial genes, a process that is sometimes referred to as lateral transduction ( Hassan et al, 2021 , Pfeifer et al, 2022 ). Unfortunately, there is no enough attention paid to horizontal transfer of new versatile ARGs of wild plant species to human gut or skin microbiome ( Chen et al, 2019 , Obermeier et al, 2021 ) although several recent reports of gene cataloging have raised such a risk ( Shami et al, 2022 , Ashy et al, 2023 ).…”