Identification of a parasitic symbiosis between respiratory metabolisms in the biogeochemical chlorine cycle

Abstract

A key step in the chlorine cycle is the reduction of perchlorate (ClO 4 -) and chlorate (ClO 3 -) to chloride by microbial respiratory pathways. Perchlorate-reducing bacteria and chlorate-reducing bacteria differ in that the latter cannot use perchlorate, the most oxidized chlorine compound.However, a recent study identified a bacterium with the chlorate reduction pathway dominating a community provided only perchlorate. Here we confirm a metabolic interaction between perchlorate-and chlorate-reducing bacteria and define its mechanism. Perchlorate-reducing bacteria supported the growth of chlorate-reducing bacteria to up to 90% of total cells in communities and co-cultures. Chlorate-reducing bacteria required the gene for chlorate reductase to grow in co-culture with perchlorate-reducing bacteria, demonstrating that chlorate is responsible for the interaction, not the subsequent intermediates chlorite and oxygen. Modeling of the interaction suggested that cells specialized for chlorate reduction have a competitive advantage for consuming chlorate produced from perchlorate, especially at high concentrations of perchlorate, because perchlorate and chlorate compete for a single enzyme in perchloratereducing cells. We conclude that perchlorate-reducing bacteria inadvertently support large populations of chlorate-reducing bacteria in a parasitic relationship through the release of the intermediate chlorate. An implication of these findings is that undetected chlorate-reducing bacteria have likely negatively impacted efforts to bioremediate perchlorate pollution for decades.

Chlorine redox chemistry is not rare in biology

“…That ancient form of dissimilatory (per)chlorate reduction may have resembled co-metabolic (per)chlorate reduction in an organism with Cld. Cld has been shown to be inessential for removing any chlorite produced if habitats have sufficient amounts of reduced inorganic sulfur species 67,68 or large populations of other organisms that can degrade chlorate or chlorite 19,61 . The above results show that chlorite stress from co-metabolic (per)chlorate reduction is a common enough phenomenon that Cld has repeatedly evolved to be co-located with co-metabolic reductase in genomes.…”

“…The copyright holder for this preprint this version posted December 8, 2021. ; https://doi.org/10.1101/2021.12.08.471835 doi: bioRxiv preprint habitats 8,18,19 . Reduction may instead occur through co-metabolism: due to the structural and chemical similarity between oxyanions like nitrate and chlorate and perchlorate, enzymes such as nitrate reductase can reduce perchlorate or chlorate 20-24 . This inadvertent reduction of perchlorate or chlorate produces chlorite and damages cells unless chlorite is degraded…”

“…The degradation of oxidized chlorine species, aside from hypochlorous acid, is thought to occur predominantly through dissimilatory (per)chlorate reduction, a specialized anaerobic respiratory pathway wherein high affinity perchlorate reductases (Pcr) or chlorate reductases (Clr) reduce perchlorate or chlorate to provide energy in anoxic habitats 8,18,19 . Reduction may instead occur through co-metabolism: due to the structural and chemical similarity between oxyanions like nitrate and chlorate and perchlorate, enzymes such as nitrate reductase can reduce perchlorate or chlorate 20-24 .…”

Halogens in Seaweeds: Biological and Environmental Significance

“…More recent reviews are available about the environmental role of fluorine [66], chlorine [67] and bromine [62].…”

“…In spite of their thermodynamic instability, the chlorine species with the highest oxidation states play a role in biology [112], because, like molecular oxygen, they combine a high thermodynamic reduction potential with kinetic inertness. Some organisms can reduce both the potentially explosive perchlorate (by perchlorate reductases [113] containing molybdenum in the active site [114]) and chlorate, others only chlorate (by chlorite reductase), both to the level of chlorite [67]. Some of the organisms that reduce perchlorate can also reduce bromate, nitrate, and iodate.…”