Non-contiguous finished genome sequence and description of Sulfurimonas hongkongensis sp. nov., a strictly anaerobic denitrifying, hydrogen- and sulfur-oxidizing chemolithoautotroph isolated from marine sediment

Lin, Chunye; Shao, Mingfei; Zhang, Tong

doi:10.4056/sigs.4948668

Cited by 34 publications

(29 citation statements)

References 23 publications

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“…P. pantotrophus , Rhodopseudomonas palustris , Rhodovulum sulfidophilum and Starkeya novella ), which carry the soxABCDXYZ genes in a single gene cluster (Ghosh and Dam, ), Sulfurimonas spp. contain two separate sox clusters, that is, soxXY 1 Z 1 AB and soxCDY 2 Z 2 (Sievert et al ., ; Sikorski et al ., ; Grote et al ., ; Cai et al ., ). Both clusters contain homologues of soxYZ , which show a high level of divergence and are proposed to be involved in oxidation of different sulfur compounds (Meier et al ., ; Pjevac et al ., ).…”

Section: Introductionmentioning

confidence: 97%

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Comparison of sulfide‐oxidizingSulfurimonasstrains reveals a new mode of thiosulfate formation in subsurface environments

Lahme

Callbeck

Eland

et al. 2020

Environmental Microbiology

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Sulfur-oxidizing Sulfurimonas spp. are widespread in sediments, hydrothermal vent fields, aquifers and subsurface environments such as oil reservoirs where they play an important role in the sulfur cycle. We determined the genome sequence of the oil field isolate Sulfurimonas sp. strain CVO and compared its gene expression during nitrate-dependent sulfide oxidation to the coastal sediment isolate Sulfurimonas denitrificans. Formation of elemental sulfur (S 0 ) and high expression of sulfide quinone oxidoreductase (SQR) genes indicates that sulfide oxidation in both strains is mediated by SQR. Subsequent oxidation of S 0 was achieved by the sulfur oxidation enzyme complex (SOX). In the coastal S. denitrificans, the genes are arranged and expressed as two clusters: soxXY 1 Z 1 AB and soxCDY 2 Z 2 H, and sulfate was the sole metabolic end product. By contrast, the oil field strain CVO has only the soxCDY 2 Z 2 H cluster and not soxXY 1 Z 1 AB. Despite the absence of the soxXY 1 Z 1 AB cluster, strain CVO oxidized S 0 to thiosulfate and sulfate, demonstrating that soxCDY 2 Z 2 H genes alone are sufficient for S 0 oxidation in Sulfurimonas spp. and that thiosulfate is an additional metabolic end product. Screening of publicly available metagenomes revealed that Sulfurimonas spp. with only the soxCDY 2 Z 2 H cluster are widespread suggesting this mechanism of thiosulfate formation is environmentally significant.

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Section: Introductionmentioning

confidence: 97%

“…Currently sequenced genomes of Sulfurimonas spp. suggest that the oxidation of reduced sulfur compounds likely involves the SOX system as well as different types of SQR enzymes (Sievert et al ., ; Sikorski et al ., ; Grote et al ., ; Cai et al ., ; Han and Perner, ). Unlike many alphaproteobacterial sulfur oxidizers (e.g.…”

Section: Introductionmentioning

confidence: 99%

Comparison of sulfide‐oxidizingSulfurimonasstrains reveals a new mode of thiosulfate formation in subsurface environments

Lahme

Callbeck

Eland

et al. 2020

Environmental Microbiology

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“…Weerakoon and Olson (2008) also showed that this unusual mechanism is due to differences in the NuoE/F subunits that interact with NADH in canonical complex I. Interestingly, they note that S. denitrificans and other autotrophic Epsilonproteobacteria also possess non-canonical NuoEF subunits. So far, this different NuoEF composition has also been observed in all genomes of Sulfurimonas and Sulfurovum sequenced to date (Nakagawa et al, 2007;Sievert et al, 2008;Sikorski et al, 2010;Grote et al, 2012;Cai et al, 2014)…”

Section: Reverse Electron Transportmentioning

confidence: 99%

“…In contrast to the Nautiliales, nearly all Campylobacterales isolates reported thus far have the potential to use oxygen, and in some cases tolerate levels approaching atmospheric concentrations Takai et al, 2006). Even for those reported to be strict anaerobes, genome sequences contain a cbb 3 -type high-affinity cytochrome c oxidase (Grote et al, 2012;Cai et al, 2014), suggesting the ability to use oxygen as an electron acceptor is typical of autotrophic Campylobacterales. The use of nitrate and sulfur as electron acceptors is also common in this lineage but obligate aerobes do exist .…”

Section: 3mentioning

confidence: 99%

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

McNichol¹

2016

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Chemoautotrophic ecosystems at deep-sea hydrothermal vents were discovered in 1977, but not until 1995 were free-living autotrophic Epsilonproteobacteria identified as important microbial community members. Because the deep-sea is food-starved, the autotrophic metabolism of hydrothermal vent Epsilonproteobacteria may be very important for deep-sea consumers. However, quantifying their metabolic activities in situ has remained difficult, and biochemical mechanisms underlying their autotrophic physiology are poorly described. To gain insight into environmental processes, an approach was developed for incubations of microbes at in situ pressure and temperature (25 MPa, 24 o C) with various combinations of electron donors/acceptors (H 2 , O 2 and NO 3 -and 13 HCO 3 -) as a tracer to track carbon fixation. During short (18-24 h) incubations of low-temperature vent fluids from Crab Spa (9 o N East Pacific Rise), the concentration of electron donors/acceptors and cell numbers were monitored to quantify microbial processes. Measured rates were generally higher than previous studies, and the stoichiometry of microbially-catalyzed redox reactions revealed new insights into sulfur and nitrogen cycling. Single-cell, taxonomically-resolved tracer incorporation showed Epsilonproteobacteria dominated carbon fixation, and their growth efficiency was calculated based on electron acceptor consumption. Using these data, in situ primary productivity, microbial standing stock, and average biomass residence time of the deep-sea vent subseafloor biosphere were estimated. Finally, the population structures of the most abundant genera Sulfurimonas and Thioreductor were shown to be strongly influenced by pO 2 and temperature respectively, providing a mechanism for niche differentiation in situ. To gain insights into the core biochemical reactions underlying autotrophy in Epsilonprotebacteria, a theoretical metabolic model of Sulfurimonas denitrificans was developed. Validated iteratively by comparing in silico yields with data from chemostat experiments, the model generated hypotheses explaining critical, yet so far unresolved reactions supporting chemoautotrophy in Epsilonproteobacteria. For example, it provides insight into how energy is conserved during sulfur oxidation coupled to denitrification, how reverse electron transport produces ferredoxin for carbon fixation, and why aerobic growth yields are only slightly higher compared to denitrification. As a whole, this thesis provides important contributions towards understanding core mechanisms of chemoautrophy, as well as the in situ productivity, physiology and ecology of autotrophic Epsilonproteobacteria.

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“…Although type II to VI sqr genes were detected in the different genome-sequenced Sulfurimonas species (20,22,(39)(40)(41), no experimental evidence for a functional SQR in Sulfurimonas currently exists. S. denitrificans harbors three sqr-homologous genes, Suden_2082, Suden_1879, and Suden_619, which encode type II, III, and IV SQRs, respectively (20,22).…”

Section: Growth Of S Denitrificans On Sulfidementioning

confidence: 99%

Sulfide Consumption in Sulfurimonas denitrificans and Heterologous Expression of Its Three Sulfide-Quinone Reductase Homologs

Han

Perner

2016

J Bacteriol

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Sulfurimonas denitrificans is a sulfur-oxidizing epsilonproteobacterium. It has been reported to grow with sulfide and to harbor genes that encode sulfide-quinone reductases (SQRs) (catalyze sulfide oxidation). However, the actual sulfide concentrations at which S. denitrificans grows and whether its SQRs are functional remain enigmatic. Here, we illustrate the sulfide concentrations at which S. denitrificans exhibits good growth, namely, 0.18 mM to roughly 1.7 mM. Around 2.23 mM, sulfide appears to inhibit growth. S. denitrificans harbors three SQR homolog genes on its genome (Suden_2082 for type II SQR, Suden_1879 for type III SQR, and Suden_619 for type IV SQR). They are all transcribed in S. denitrificans. According to our experiments, they appear to be loosely bound to the membrane. Each individual S. denitrificans SQR was heterologously expressed in the Rhodobacter capsulatus SB1003 sqr deletion mutant, and all exhibited SQR activities individually. This suggests that all of these three genes encode functional SQRs. This study also provides the first experimental evidence of a functional bacterial type III SQR. IMPORTANCEAlthough the epsilonproteobacterium Sulfurimonas denitrificans has been described as using many reduced sulfur compounds as electron donors, there is little knowledge about its growth with sulfide. In many bacteria, the sulfide-quinone reductase (SQR) is responsible for catalyzing sulfide oxidation. S. denitrificans has an array of different types of sqr genes on its genome and so do several other sulfur-oxidizing Epsilonproteobacteria. However, whether these SQRs are functional has remained unknown. Here, we shed light on sulfide metabolism in S. denitrificans. Our study provides the first experimental evidence of active epsilonproteobacterial SQRs and also gives the first report of a functional bacterial type III SQR. Sulfide is a reduced sulfur compound present in nature (e.g., marine sediments and hydrothermal deep-sea vents [1-4]), and it can serve as an electron donor for many bacteria in their phototrophic and chemolithotrophic growth. Two enzymes have been reported for the oxidation of sulfide, sulfide-quinone reductase (SQR; EC 1.8.5.4) and flavocytochrome c (FCC; also known as sulfide-cytochrome c oxidoreductase). The electrons released from the oxidation of sulfide enter the photo-and chemolithotrophic electron transport chain either at the level of the quinone pool via SQR or at the level of cytochrome c via FCC (5). The two enzymes are sulfide-oxidizing flavoproteins, but metabolic energy generation with SQR is more efficient than that with FCC (5).SQRs are globally distributed and present in all three kingdoms (6-16). According to their structure-based sequence fingerprints, SQR enzymes have been classified into six types (i.e., SQR types I to VI) (16). In the last two decades, many of these SQR types have been studied in detail, e.g., type I SQRs from the alphaproteobacteria Rhodobacter capsulatus (6) and Paracoccus denitrificans (15), type II SQR from the nonpathoge...

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Non-contiguous finished genome sequence and description of Sulfurimonas hongkongensis sp. nov., a strictly anaerobic denitrifying, hydrogen- and sulfur-oxidizing chemolithoautotroph isolated from marine sediment

Cited by 34 publications

References 23 publications

Comparison of sulfide‐oxidizingSulfurimonasstrains reveals a new mode of thiosulfate formation in subsurface environments

Comparison of sulfide‐oxidizingSulfurimonasstrains reveals a new mode of thiosulfate formation in subsurface environments

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

Sulfide Consumption in Sulfurimonas denitrificans and Heterologous Expression of Its Three Sulfide-Quinone Reductase Homologs

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