Requirements for Efficient Thiosulfate Oxidation in Bradyrhizobium diazoefficiens

Masuda, Sachiko; Hennecke, Hauke; Fischer, Hans‐Martin

doi:10.3390/genes8120390

Cited by 4 publications

(3 citation statements)

References 30 publications

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“…The organization of soxABYZX genes and their regulators into a single operon, as we saw in Sedimenticola , was previously observed in free-living SOB such as P. pantotrophus , Chlorobium tepidum , Bradyrhizobium diazoefficiens , and A. thiooxidans ( 91 – 93 ). An operon structure would enable co-regulation and co-transcription of the entire Sox pathway, minimizing stochastic variations in gene expression and reducing the regulatory information required for optimizing gene expression patterns ( 94 , 95 ).…”

Section: Discussionsupporting

confidence: 73%

SoxY gene family expansion underpins adaptation to diverse hosts and environments in symbiotic sulfide oxidizers

Sudo,

Osvatic,

Taylor

et al. 2024

mSystems

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Sulfur-oxidizing bacteria (SOB) have developed distinct ecological strategies to obtain reduced sulfur compounds for growth. These range from specialists that can only use a limited range of reduced sulfur compounds to generalists that can use many different forms as electron donors. Forming intimate symbioses with animal hosts is another highly successful ecological strategy for SOB, as animals, through their behavior and physiology, can enable access to sulfur compounds. Symbioses have evolved multiple times in a range of animal hosts and from several lineages of SOB. They have successfully colonized a wide range of habitats, from seagrass beds to hydrothermal vents, with varying availability of symbiont energy sources. Our extensive analyses of sulfur transformation pathways in 234 genomes of symbiotic and free-living SOB revealed widespread conservation in metabolic pathways for sulfur oxidation in symbionts from different host species and environments, raising the question of how they have adapted to such a wide range of distinct habitats. We discovered a gene family expansion of soxY in these genomes, with up to five distinct copies per genome. Symbionts harboring only the “canonical” soxY were typically ecological “specialists” that are associated with specific host subfamilies or environments (e.g., hydrothermal vents, mangroves). Conversely, symbionts with multiple divergent soxY genes formed versatile associations across diverse hosts in various marine environments. We hypothesize that expansion and diversification of the soxY gene family could be one genomic mechanism supporting the metabolic flexibility of symbiotic SOB enabling them and their hosts to thrive in a range of different and dynamic environments. IMPORTANCE Sulfur metabolism is thought to be one of the most ancient mechanisms for energy generation in microorganisms. A diverse range of microorganisms today rely on sulfur oxidation for their metabolism. They can be free-living, or they can live in symbiosis with animal hosts, where they power entire ecosystems in the absence of light, such as in the deep sea. In the millions of years since they evolved, sulfur-oxidizing bacteria have adopted several highly successful strategies; some are ecological “specialists,” and some are “generalists,” but which genetic features underpin these ecological strategies are not well understood. We discovered a gene family that has become expanded in those species that also seem to be “generalists,” revealing that duplication, repurposing, and reshuffling existing genes can be a powerful mechanism driving ecological lifestyle shifts.

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Section: Discussionsupporting

confidence: 73%

SoxY gene family expansion underpins adaptation to diverse hosts and environments in symbiotic sulfide oxidizers

Sudo,

Osvatic,

Taylor

et al. 2024

mSystems

View full text Add to dashboard Cite

show abstract

“…Importantly, the cycA mutant retained partial N 2 OR activity, which suggests that alternative electron donors might be also involved in electron transfer to Nos. This has been observed in other model denitrifying bacteria (reviewed in van Spanning, 2011; Torres et al, 2016) and the presence of alternative electron transfer routes was also proposed for chemolithoautotrophic growth as reported by Masuda et al (2017). To identify other candidates as potential electron donors to Nos, we determined N 2 OR activity in B. diazoefficiens strains defective in the soluble cytochromes c 2 encoded by bll2388 and CycS encoded by bll6062 (Mesa et al, 2008).…”

Section: Discussionmentioning

confidence: 54%

“…We have now reported, for the first time in B. diazoefficiens , the role of CycA in nitrous oxide reductase functioning, given the reduced N 2 OR activity observed in the cycA mutant compared to that of the WT. In addition to its involvement in the denitrification process, CycA plays a role in chemolithotrophic growth of B. diazoefficiens when thiosulfate is used as electron donor (Masuda et al, 2017). In this growth condition, electrons are preferentially channeled via cytochrome CycA to the aa 3 -type heme-copper cytochrome oxidase encoded by coxBAFC genes.…”

Section: Discussionmentioning

confidence: 99%

Expanding the Regulon of the Bradyrhizobium diazoefficiens NnrR Transcription Factor: New Insights Into the Denitrification Pathway

et al. 2019

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Denitrification in the soybean endosymbiont Bradyrhizobium diazoefficiens is controlled by a complex regulatory network composed of two hierarchical cascades, FixLJ-FixK 2 -NnrR and RegSR-NifA. In the former cascade, the CRP/FNR-type transcription factors FixK 2 and NnrR exert disparate control on expression of core denitrifying systems encoded by napEDABC , nirK , norCBQD , and nosRZDFYLX genes in response to microoxia and nitrogen oxides, respectively. To identify additional genes controlled by NnrR and involved in the denitrification process in B. diazoefficiens , we compared the transcriptional profile of an nnrR mutant with that of the wild type, both grown under anoxic denitrifying conditions. This approach revealed more than 170 genes were simultaneously induced in the wild type and under the positive control of NnrR. Among them, we found the cycA gene which codes for the c 550 soluble cytochrome (CycA), previously identified as an intermediate electron donor between the bc 1 complex and the denitrifying nitrite reductase NirK. Here, we demonstrated that CycA is also required for nitrous oxide reductase activity. However, mutation in cycA neither affected nosZ gene expression nor NosZ protein steady-state levels. Furthermore, cycA , nnrR and its proximal divergently oriented nnrS gene, are direct targets for FixK 2 as determined by in vitro transcription activation assays. The dependence of cycA expression on FixK 2 and NnrR in anoxic denitrifying conditions was validated at transcriptional level, determined by quantitative reverse transcription PCR, and at the level of protein by performing heme c -staining of soluble cytochromes. Thus, this study expands the regulon of NnrR and demonstrates the role of CycA in the activity of the nitrous oxide reductase, the key enzyme for nitrous oxide mitigation.

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Orchestration of the Plant Microbiome for Enhanced Agriculture

Sharma

2023

Sustainable Agriculture Reviews

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Requirements for Efficient Thiosulfate Oxidation in Bradyrhizobium diazoefficiens

Cited by 4 publications

References 30 publications

SoxY gene family expansion underpins adaptation to diverse hosts and environments in symbiotic sulfide oxidizers

SoxY gene family expansion underpins adaptation to diverse hosts and environments in symbiotic sulfide oxidizers

Expanding the Regulon of the Bradyrhizobium diazoefficiens NnrR Transcription Factor: New Insights Into the Denitrification Pathway

Orchestration of the Plant Microbiome for Enhanced Agriculture

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