Organohalide-respiring Desulfoluna species isolated from marine environments

Peng Peng,Bart Nijsse,Detmer Sipkema,Alfons J M Stams,Jie Liu,Hauke Smidt,Jaap S Sinninghe Damste,Yue Lu,Anna Burrichter,Jasper J Koehorst,Max M Häggblom,David Schleheck,Siavash Atashgahi,Tobias Goris

doi:10.1038/s41396-019-0573-y

Abstract

The genus Desulfoluna comprises two anaerobic sulfate-reducing strains, D. spongiiphila AA1T and D. butyratoxydans MSL71T, of which only the former was shown to perform organohalide respiration (OHR). Here we isolated a third strain, designated D. spongiiphila strain DBB, from marine intertidal sediment using 1,4-dibromobenzene and sulfate as the electron acceptors and lactate as the electron donor. Each strain harbors three reductive dehalogenase gene clusters (rdhABC) and corrinoid biosynthesis genes in their genomes, and dehalogenated brominated but not chlorinated organohalogens. The Desulfoluna strains maintained OHR in the presence of 20 mM sulfate or 20 mM sulfide, which often negatively affect other organohalide-respiring bacteria. Strain DBB sustained OHR with 2% oxygen in the gas phase, in line with its genetic potential for reactive oxygen species detoxification. Reverse transcription-quantitative PCR revealed differential induction of rdhA genes in strain DBB in response to 1,4-dibromobenzene or 2,6-dibromophenol. Proteomic analysis confirmed expression of rdhA1 with 1,4-dibromobenzene, and revealed a partially shared electron transport chain from lactate to 1,4-dibromobenzene and sulfate, which may explain accelerated OHR during concurrent sulfate reduction. Versatility in using electron donors, de novo corrinoid biosynthesis, resistance to sulfate, sulfide and oxygen, and concurrent sulfate reduction and OHR may confer an advantage to marine Desulfoluna strains.

Highlights

IntroductionDuring organohalide respiration (OHR) organohalogens are used as terminal electron acceptors, and their reductive dehalogenation is coupled to energy conservation [8,9,10]
Supplementary information The online version of this article contains supplementary material, which is available to authorized users.More than 5000 naturally produced organohalides have been identified, some of which have already been present in a variety of environments for millions of years [1]
Our results showed that resistance of Desulfoluna strains to sulfide was remarkable among the reported sulfate-reducing bacteria, and concurrent reduction of sulfate and organohalogens as terminal electron acceptors was unique among the currently known organohalide-respiring bacteria (OHRB)

Summary

Introduction

During organohalide respiration (OHR) organohalogens are used as terminal electron acceptors, and their reductive dehalogenation is coupled to energy conservation [8,9,10]. This process is mediated by reductive dehalogenases (RDases), which are membrane-associated, corrinoiddependent, and oxygen-sensitive proteins [9,10,11]. The corresponding rdh gene clusters usually consist of rdhA encoding the catalytic subunit, rdhB encoding a putative membrane anchor protein [10], and a variable set of accessory genes encoding RdhC and other proteins likely involved in regulation, maturation and/or electron transport [12, 13]. Recent studies suggested that RdhC may serve as electron carrier during OHR in Firmicutes [15, 16]

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