Rhodococcus erythropolis MTHt3 biotransforms ergopeptines to lysergic acid

Abstract

BackgroundErgopeptines are a predominant class of ergot alkaloids produced by tall fescue grass endophyte Neotyphodium coenophialum or cereal pathogen Claviceps purpurea. The vasoconstrictive activity of ergopeptines makes them toxic for mammals, and they can be a problem in animal husbandry.ResultsWe isolated an ergopeptine degrading bacterial strain, MTHt3, and classified it, based on its 16S rDNA sequence, as a strain of Rhodococcus erythropolis (Nocardiaceae, Actinobacteria). For strain isolation, mixed microbial cultures were obtained from artificially ergot alkaloid-enriched soil, and provided with the ergopeptine ergotamine in mineral medium for enrichment. Individual colonies derived from such mixed cultures were screened for ergotamine degradation by high performance liquid chromatography and fluorescence detection. R. erythropolis MTHt3 converted ergotamine to ergine (lysergic acid amide) and further to lysergic acid, which accumulated as an end product. No other tested R. erythropolis strain degraded ergotamine. R. erythropolis MTHt3 degraded all ergopeptines found in an ergot extract, namely ergotamine, ergovaline, ergocristine, ergocryptine, ergocornine, and ergosine, but the simpler lysergic acid derivatives agroclavine, chanoclavine, and ergometrine were not degraded. Temperature and pH dependence of ergotamine and ergine bioconversion activity was different for the two reactions.ConclusionsDegradation of ergopeptines to ergine is a previously unknown microbial reaction. The reaction end product, lysergic acid, has no or much lower vasoconstrictive activity than ergopeptines. If the genes encoding enzymes for ergopeptine catabolism can be cloned and expressed in recombinant hosts, application of ergopeptine and ergine degrading enzymes for reduction of toxicity of ergot alkaloid-contaminated animal feed may be feasible.

Beef cattle that respond differently to fescue toxicosis have distinct gastrointestinal tract microbiota

“…degrade ergot alkaloids [21]. We found only very few and extremely low abundant Rhodococcus OTUs in our dataset; based on the reported strain-specific ergot alkaloid degradation capability of Rhodococcus [21], we assume that Rhodococcus species are not involved in ergot alkaloid degradation in the animals analyzed here. We chose to study the fecal microbiota as fecal samples allow for periodic observations of microbiota with large sample sizes in a non-invasive way.…”

“…Another explanation for the absence of Prevotella bryantii and Clostridium sporogenes , which are abundant rumen bacteria, in our samples might be that we have used fecal (and not rumen) samples and rumen bacteria might not be well represented in fecal samples. Additionally, a Rhodococcus erythropolis strain has recently been described to degrade ergot alkaloids [ 21 ]. We found only very few and extremely low abundant Rhodococcus OTUs in our dataset; based on the reported strain-specific ergot alkaloid degradation capability of Rhodococcus [ 21 ], we assume that Rhodococcus species are not involved in ergot alkaloid degradation in the animals analyzed here.…”

“…Additionally, a Rhodococcus erythropolis strain has recently been described to degrade ergot alkaloids [ 21 ]. We found only very few and extremely low abundant Rhodococcus OTUs in our dataset; based on the reported strain-specific ergot alkaloid degradation capability of Rhodococcus [ 21 ], we assume that Rhodococcus species are not involved in ergot alkaloid degradation in the animals analyzed here.…”

“…Most recently, Mote et al surveyed fecal bacterial communities of beef cattle during a FT challenge, and described possible connections between the abundance of certain bacterial phylotypes and the host response to FT [17]. Other studies have suggested microbial communities within the cow rumen [18,19], earthworm's intestine [20], and soil [21] are able to degrade ergovaline. It is thus conceivable that the GI tract microbiota may be able to reduce the toxic effect of ergot alkaloids and thus mitigate some of the impact of FT symptoms on livestock.…”

Beef cattle that respond differently to fescue toxicosis have distinct gastrointestinal tract microbiota

“…The current literature published on the effect of toxic tall fescue effects on gastrointestinal (GI) microbiota is still limited. Most recently, Mote et al, 2019 [17] surveyed fecal bacterial communities of beef cattle during a FT challenge, and described possible connections between the abundance of certain bacterial phylotypes and the host response to FT. Other studies have suggested microbial communities within the cow rumen [18, 19], earthworm’s intestine [20], and soil [21] are able to degrade ergovaline. It is thus conceivable that the GI tract microbiota may be able to alleviate some of the impact of FT symptoms.…”