Organohalide respiration in pristine environments: implications for the natural halogen cycle

Abstract

Summary Halogenated organic compounds, also termed organohalogens, were initially considered to be of almost exclusively anthropogenic origin. However, over 5000 naturally synthesized organohalogens are known today. This has also fuelled the hypothesis that the natural and ancient origin of organohalogens could have primed development of metabolic machineries for their degradation, especially in microorganisms. Among these, a special group of anaerobic microorganisms was discovered that could conserve energy by reducing organohalogens as terminal electron acceptor in a process termed organohalide respiration. Originally discovered in a quest for biodegradation of anthropogenic organohalogens, these organohalide‐respiring bacteria (OHRB) were soon found to reside in pristine environments, such as the deep subseafloor and Arctic tundra soil with limited/no connections to anthropogenic activities. As such, accumulating evidence suggests an important role of OHRB in local natural halogen cycles, presumably taking advantage of natural organohalogens. In this minireview, we integrate current knowledge regarding the natural origin and occurrence of industrially important organohalogens and the evolution and spread of OHRB, and describe potential implications for natural halogen and carbon cycles.

Organohalide-respiringDesulfolunaspecies isolated from marine environments

“…S6). This may indicate a cytoplasmic localization and a non-respiratory role of the RdhA1 in strain MSL71 ⊤ [6].…”

“…Widespread environmental contamination with organohalogen compounds and their harmful impacts to human and environmental health has been the driver of chasing OHRB since the 1970s. In addition, the environment itself is an ample and ancient source of natural organohalogens, and accumulating evidence shows widespread occurrence of rdhA in marine environments [6]. The previous isolation and description of strain AA1 ⊤ from a marine sponge, the isolation of strain DBB from intertidal sediment samples, and verification of the OHR potential of strain MSL71 ⊤ in this study indicate niche specialization of the members of the genus Desulfoluna as chemoorganotrophic facultative OHRB in marine environments rich in sulfate and organohalogens.…”

“…In particular, marine environments are a rich source of chlorinated, brominated and iodinated organohalides produced by marine algae, seaweeds, sponges, and bacteria [2], Fenton-like [3] and photochemical reactions, as well as volcanic activities [4, 5]. Such a natural and ancient presence of organohalogens in marine environments may have primed development of various microbial dehalogenation metabolisms [6]. Furthermore, marine environments and coastal regions in particular are also commonly reported to be contaminated with organohalogens from anthropogenic sources [7].…”

“…Desulfitobacterium hafniense) are generalists with a versatile metabolism [17, 18]. Numerous studies have reported OHR activity and occurrence of OHRB and rdhA genes in marine environments [6, 19–21]. Recent genomic [22–24] and single-cell genomic [25] analyses revealed widespread occurrence of rdh gene clusters in marine Deltaproteobacteria , indicting untapped potential for OHR.…”

Chloromethane Degradation in Soils: A Combined Microbial and Two‐Dimensional Stable Isotope Approach

“…Thus, it was puzzling to find enriched taxa affiliated with Chloroflexi , since no evidence for methylotrophy has been detected so far for representatives of Chloroflexi in grassland soils (Butterfield et al, 2016). Nonetheless, Chloroflexi were predominant in environments containing methane (Vaksmaa et al, 2017; Vigneron et al, 2017) and displayed a wide range of catabolic abilities including anaerobic dehlalogenation (Löffler et al, 2013; Atashgahi et al, 2017). This suggests that ecologically relevant taxa other than the already characterized CH 3 Cl‐degrading strains isolated under laboratory conditions may contribute to the in situ microbial response to CH 3 Cl emissions in soils.…”