Microbial pathway for anaerobic 5′-methylthioadenosine metabolism coupled to ethylene formation

Abstract

SignificanceSulfur is an essential element required by all organisms. Therefore, salvage of wasteful, sulfur-containing cellular by-products can be critical. Methionine salvage pathways for organisms living in oxic environments are well established. However, if and by what mechanisms organisms living in anoxic environments can regenerate methionine from such by-products remain largely unknown. This work identifies a strictly anaerobic methionine salvage pathway, the key genes for which appear to be widespread among obligate and facultatively anaerobic bacteria. Strikingly, this pathway also results in the formation of ethylene gas, a key plant hormone and signaling molecule. Anoxic environments routinely accumulate biologically produced ethylene at significant levels, but the organisms and mechanisms responsible have been slow to emerge. This study provides one possible route.

Revisiting the methionine salvage pathway and its paralogues

“…However, the strongest argument pleading in favour of a paralogous pathway in strain S88 is the following. The gene product annotated as the counterpart of MtnB (ECS88_4903) is in fact remarkably similar to aldolase Ald2 that has been proposed to enter the anaerobic ethylene pathway in R. rubrum (North et al ., , Fig. ).…”

“…A solution to this challenging question may come from the identification of a second catabolic pathway involving MTRu‐1‐P, found both in R. palustris and R. rubrum (North et al ., ). This pathway, named the ‘DHAP‐ethylene shunt’ is exclusively anaerobic (Miller et al ., ).…”

“…In this organism, the 2‐(methylthio)acetaldehyde formed by the aldolase is subsequently reduced by an alcohol dehydrogenase – there are many candidates with this activity in most genomes – to 2‐(methylthio)ethanol. Here, this metabolite is further metabolized by unknown enzymes to recycle the methylthio‐ moiety, while generating ethylene (North et al ., ; Miller et al ., ). The methanethiol product made here – by a still unknown anaerobic pathway – could be directly utilized by O ‐acyl‐ l ‐homoserine sulphhydrylase to regenerate methionine as described previously.…”

“…Instead, a MTRu-1-P 1,3-isomerase, highly similar to RuBisCO/ MtnW, catalysed isomerization of 5-methylthio-D-ribulose-1-phosphate (MTRu1-P) to a 3:1 mixture of 1-methylthio-D-xylulose-5-phosphate (MTXu-5-P) and methylthio-Dribulose-1-phosphate (note the 'inverted' numbering, discussed in Imker et al, 2008). In turn, this mixture entered a reductive pathway, the details of which are still being explored (Erb et al, 2012;North et al, 2017), involving a MTXu-5-P methylsulphurylase, a member of the cupin superfamily (Uberto and Moomaw, 2013). This enzyme produced methanethiol and 1-deoxy-D-xylulose-5-P (DXP, Warlick et al, 2012b), the key precursor of isoprenoids in bacteria (Dickschat, 2011).…”

“…This suggested therefore that this intermediate was metabolized via an unknown pathway or that it was involved in a paralogous pathway, as illustrated previously with the example of M. jannaschii. A solution to this challenging question may come from the identification of a second catabolic pathway involving MTRu-1-P, found both in R. palustris and R. rubrum (North et al, 2017). This pathway, named the 'DHAPethylene shunt' is exclusively anaerobic (Miller et al, 2018a).…”