Lateral Transfer of the Denitrification Pathway Genes among
            <i>Thermus thermophilus</i>
            Strains

Álvarez, Laura; Bricio, Carlos; Gómez, Manuel J.; Berenguer, José

doi:10.1128/aem.02048-10

Cited by 33 publications

(44 citation statements)

References 34 publications

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“…obically (PRQ25 or NAR1) can transfer such a property to the aerobic HB27 strain by cell-to-cell contacts (21,41). In such cases, differences among membrane protein patterns provide the easiest way to identify donor and recipient strains, as shown in Fig.…”

Section: Figmentioning

confidence: 99%

Noncanonical Cell-to-Cell DNA Transfer in Thermus spp. Is Insensitive to Argonaute-Mediated Interference

et al. 2015

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bHorizontal gene transfer drives the rapid evolution of bacterial populations. Classical processes that promote the lateral flow of genetic information are conserved throughout the prokaryotic world. However, some species have nonconserved transfer mechanisms that are not well known. This is the case for the ancient extreme thermophile Thermus thermophilus. In this work, we show that T. thermophilus strains are capable of exchanging large DNA fragments by a novel mechanism that requires cell-tocell contacts and employs components of the natural transformation machinery. This process facilitates the bidirectional transfer of virtually any DNA locus but favors by 10-fold loci found in the megaplasmid over those in the chromosome. In contrast to naked DNA acquisition by transformation, the system does not activate the recently described DNA-DNA interference mechanism mediated by the prokaryotic Argonaute protein, thus allowing the organism to distinguish between DNA transferred from a mate and exogenous DNA acquired from unknown hosts. This Argonaute-mediated discrimination may be tentatively viewed as a strategy for safe sharing of potentially "useful" traits by the components of a given population of Thermus spp. without increasing the genome sizes of its individuals. L ateral gene flow is responsible for the enormous plasticity observed in prokaryotic genomes, which confers on these organisms the ability to adapt rapidly to environmental changes (1-5). Three conserved mechanisms are traditionally associated with lateral gene transfer (LGT) in prokaryotes: phage-mediated transduction, natural transformation, and conjugation. Besides, alternative DNA transfer systems based on nanotubes (6), membrane vesicles, and nanopods in Archaea (7-9), or on the so-called "gene transfer agents" (10), have been described as contributors to genetic exchange among prokaryotes. Among these processes, transformation and conjugation depend only on functions encoded by the bacterial cell. Transformation involves the uptake of naked DNA from the environment and relies entirely on the ability of a competent recipient cell to incorporate DNA. Conjugation, on the other hand, is traditionally seen as the unidirectional transfer of a plasmid DNA molecule from a donor to a recipient cell, where the proteins responsible for DNA transfer are provided exclusively by the donor cell (11).Conjugation differs from transformation not only in the imperative need for a mate for the transfer of DNA but also in the nature of the transferred DNA. While transformation can be envisioned as a mechanism that might have originally evolved in ancestral bacteria, such as Thermus spp., for the acquisition of DNA of any sort and origin as a nutrient, conjugation is more frequently associated with a gain of new capabilities from related species and commonly involves plasmids or megaplasmids that encode all the functions required for conjugation. In fact, transfer of chromosomal genes is apparently less common and in many cases requires the integration of a conjug...

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Section: Figmentioning

confidence: 99%

Noncanonical Cell-to-Cell DNA Transfer in Thermus spp. Is Insensitive to Argonaute-Mediated Interference

et al. 2015

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“…The nic cluster can be laterally transferred only to PD strains, because the expression of its genes is dependent on the presence of the NCE in the recipient strain (13). Actually, in CD strains, the NCE and the nic clusters are located close to each other in a region of the pTT27 megaplasmid surrounded by insertion sequences, which putatively could facilitate its dissemination as a mobile denitrification genetic island among T. thermophilus strains (11,13).…”

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“…Among the latter, there is also strain variability, and some of these strains can grow anaerobically with only nitrate with final production of nitrite (partially denitrificant [PD] strains), whereas other strains can also respire nitrite with production of nitrogen gas (completely denitrificant [CD] strains) (11). Nitrate respiration is encoded by the nitrate conjugative element (NCE), a genetic element that can be transferred from PD or CD strains to aerobic strain HB27 (12,13). The NCE encodes a complete set of genes for nitrate respiration, including a nitrate reductase (Nar), a dedicated NADH dehydrogenase (Nrc) (14,15), nitrate and nitrite transporters (NarK and NarT), and signal transduction systems required for expression under appropriate conditions, which are unrelated to those found in proteobacteria or Gram-positive organisms (DnrS and DnrT) (reviewed in reference 11).…”

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“…In this work, we analyze the role in nitrite respiration of three genes of the nic cluster (nirS, nirJ, and nirM) that encode homologues of proteins involved in nitrite respiration in other bacteria (13). Our data show that NirS, the homologue of cd 1 nitrite reductases, is actually involved in nitrite reduction during denitrification but that in its absence, an alternative nitrite-reducing activity exists, with the presence of the nitrate reductase (Nar) being required for both pathways.…”

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Parallel Pathways for Nitrite Reduction during Anaerobic Growth in Thermus thermophilus

et al. 2014

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Respiratory reduction of nitrate and nitrite is encoded in Thermus thermophilus by the respective transferable gene clusters. Nitrate is reduced by a heterotetrameric nitrate reductase (Nar) encoded along transporters and regulatory signal transduction systems within the nitrate respiration conjugative element (NCE). The nitrite respiration cluster (nic) encodes homologues of nitrite reductase (Nir) and nitric oxide reductase (Nor). The expression and role of the nirSJM genes in nitrite respiration were analyzed. The three genes are expressed from two promoters, one (nirSp) producing a tricistronic mRNA under aerobic and anaerobic conditions and the other (nirJp) producing a bicistronic mRNA only under conditions of anoxia plus a nitrogen oxide. As for its nitrite reductase homologues, NirS is expressed in the periplasm, has a covalently bound heme c, and conserves the heme d 1 binding pocket. NirJ is a cytoplasmic protein likely required for heme d 1 synthesis and NirS maturation. NirM is a soluble periplasmic homologue of cytochrome c 552 . Mutants defective in nirS show normal anaerobic growth with nitrite and nitrate, supporting the existence of an alternative Nir in the cells. Gene knockout analysis of different candidate genes did not allow us to identify this alternative Nir protein but revealed the requirement for Nar in NirS-dependent and NirS-independent nitrite reduction. As the likely role for Nar in the process is in electron transport through its additional cytochrome c periplasmic subunit (NarC), we concluded all the Nir activity takes place in the periplasm by parallel pathways.

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“…The most characterized strains belonging to the Thermus genus are strict aerobes; however, a few isolates have been shown to be facultative anaerobes, growing by reducing nitrate to nitrite (nitrate reduction) or by reducing nitrate and nitrite to either N 2 O (incomplete denitrification) or N 2 (complete denitrification) (24). Denitrifying Thermus thermophilus strains are a contributor of the N 2 O released from thermal systems (24), and in this work the operon encoding the enzyme responsible for this has been cloned from the denitrifying strain T. thermophilus PRQ25 (25) and has been expressed in both T. thermophilus and Escherichia coli.…”

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Characterization of the nitric oxide reductase from Thermus thermophilus

Schurig-Briccio

Venkatakrishnan

Hemp

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Nitrous oxide (N 2 O) is a powerful greenhouse gas implicated in climate change. The dominant source of atmospheric N 2 O is incomplete biological dentrification, and the enzymes responsible for the release of N 2 O are NO reductases. It was recently reported that ambient emissions of N 2 O from the Great Boiling Spring in the United States Great Basin are high, and attributed to incomplete denitrification by Thermus thermophilus and related bacterial species [Hedlund BP, et al. (2011) Geobiology 9(6)471–480]. In the present work, we have isolated and characterized the NO reductase (NOR) from T. thermophilus . The enzyme is a member of the cNOR family of enzymes and belongs to a phylogenetic clade that is distinct from previously examined cNORs. Like other characterized cNORs, the T. thermophilus cNOR consists of two subunits, NorB and NorC, and contains a one heme c , one Ca 2+ , a low-spin heme b , and an active site consisting of a high-spin heme b and Fe B . The roles of conserved residues within the cNOR family were investigated by site-directed mutagenesis. The most important and unexpected result is that the glutamic acid ligand to Fe B is not essential for function. The E211A mutant retains 68% of wild-type activity. Mutagenesis data and the pattern of conserved residues suggest that there is probably not a single pathway for proton delivery from the periplasm to the active site that is shared by all cNORs, and that there may be multiple pathways within the T. thermophilus cNOR.

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Lateral Transfer of the Denitrification Pathway Genes among Thermus thermophilus Strains

Cited by 33 publications

References 34 publications

Noncanonical Cell-to-Cell DNA Transfer in Thermus spp. Is Insensitive to Argonaute-Mediated Interference

Noncanonical Cell-to-Cell DNA Transfer in Thermus spp. Is Insensitive to Argonaute-Mediated Interference

Parallel Pathways for Nitrite Reduction during Anaerobic Growth in Thermus thermophilus

Characterization of the nitric oxide reductase from Thermus thermophilus

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