Potassium permanganate elicits a shift of the external fish microbiome and increases host susceptibility to columnaris disease

Abstract

The external microbiome of fish is thought to benefit the host by hindering the invasion of opportunistic pathogens and/or stimulating the immune system. Disruption of those microbial communities could increase susceptibility to diseases. Traditional aquaculture practices include the use of potent surface-acting disinfectants such as potassium permanganate (PP, KMnO4) to treat external infections. This study evaluated the effect of PP on the external microbiome of channel catfish and investigated if dysbiosis leads to an increase in disease susceptibility. Columnaris disease, caused by Flavobacterium columnare, was used as disease model. Four treatments were compared in the study: (I) negative control (not treated with PP nor challenged with F. columnare), (II) treated but not challenged, (III) not treated but challenged, and (IV) treated and challenged. Ribosomal intergenic spacer analysis (RISA) and pyrosequencing were used to analyze changes in the external microbiome during the experiment. Exposure to PP significantly disturbed the external microbiomes and increased catfish mortality following the experimental challenge. Analysis of similarities of RISA profiles showed statistically significant changes in the skin and gill microbiomes based on treatment and sampling time. Characterization of the microbiomes using 16S rRNA gene pyrosequencing confirmed the disruption of the skin microbiome by PP at different phylogenetic levels. Loss of diversity occurred during the study, even in the control group, but was more noticeable in fish subjected to PP than in those challenged with F. columnare. Fish treated with PP and challenged with the pathogen exhibited the least diverse microbiome at the end of the study.

Fish are not alone: characterization of the gut and skin microbiomes of Largemouth Bass (Micropterus salmoides), Bluegill (Lepomis macrochirus), and Spotted Gar (Lepisosteus oculatus)

“…The composition at the phylum level of the bacterial communities found in association with fish skin that we described in this study was consistent with previous findings from skin and mucus of various fish taxa including freshwater and saltwater environments (Cipriano and Dove, 2009;Arias et al, 2013;Larsen et al, 2013;Larsen et al, 2015;Mohammed and Arias, 2015). However, at the genus level, there were some surprising results, as Cetobacterium (19.33%) was found to be the most abundant genus overall for skin communities of the three species (Table 4).…”

The Inner Workings of the Outer Surface: Skin and Gill Microbiota as Indicators of Changing Gut Health in Yellowtail Kingfish

“…A further shift in the community between the early and later stages of enteritis was observed, with a reduction in the abundance of these early stage enriched taxa and a concomitant increase in overall diversity similar to the healthy fish. Studies on other teleosts have also noted a change in the skin and gill microbiota in response to underlying stressors ( Roberts and Powell, 2005 ; Hess et al, 2015 ; Mohammed and Arias, 2015 ). Interestingly, the α-subdivision of the Proteobacteria which inhabit a wide range of ecosystems and have become adapted to eukaryotic hosts where they form both extra- and intracellular associations, has evolved an array of chronic infection strategies ( Batut et al, 2004 ).…”

Transition from freshwater to seawater reshapes the skin-associated microbiota of Atlantic salmon

“…Skin and its mucosa are the primary barriers in the defence of fish 6 . Any change in the rearing environment of the fish is likely to affect the skin-associated microbial balance 4 7 8 . Therefore, in the present study we investigated the shift in the skin-associated bacterial community of Atlantic salmon caused by the transfer of the fish from freshwater to seawater.…”