TonB-Dependent Receptors in Nitrogen-Fixing Nodulating Bacteria

Lim, Boon Leong

doi:10.1264/jsme2.me10102

Cited by 27 publications

(24 citation statements)

References 53 publications

(61 reference statements)

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“…Under low-iron conditions, the growth of the ⌬irrB strain was significantly reduced and the bhuA gene was downregulated, findings similar to those for A. tumefaciens and Brucella abortus (26,27). In MSR-1, bhuA is annotated as a putative TonB-dependent receptor that is located in the outer membranes and facilitates the acquisition of scarce resources in an energy-dependent manner (28). These findings suggest that IrrB is required for the induction of bhuA transcription in response to low-iron conditions and that irrB deletion disrupts iron uptake.…”

Section: Discussionsupporting

confidence: 60%

Iron Response Regulator Protein IrrB in Magnetospirillum gryphiswaldense MSR-1 Helps Control the Iron/Oxygen Balance, Oxidative Stress Tolerance, and Magnetosome Formation

Wang

et al. 2015

Appl Environ Microbiol

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cMagnetotactic bacteria are capable of forming nanosized, membrane-enclosed magnetosomes under iron-rich and oxygen-limited conditions. The complete genomic sequence of Magnetospirillum gryphiswaldense strain MSR-1 has been analyzed and found to contain five fur homologue genes whose protein products are predicted to be involved in iron homeostasis and the response to oxidative stress. Of these, only the MGMSRv2_3149 gene (irrB) was significantly downregulated under high-iron and low-oxygen conditions, during the transition of cell growth from the logarithmic to the stationary phase. The encoded protein, IrrB, containing the conserved HHH motif, was identified as an iron response regulator (Irr) protein belonging to the Fur superfamily. To investigate the function of IrrB, we constructed an irrB deletion mutant (⌬irrB). The levels of cell growth and magnetosome formation were lower in the ⌬irrB strain than in the wild type (WT) under both high-iron and low-iron conditions. The ⌬irrB strain also showed lower levels of iron uptake and H 2 O 2 tolerance than the WT. Quantitative real-time reverse transcription-PCR analysis indicated that the irrB mutation reduced the expression of numerous genes involved in iron transport, iron storage, heme biosynthesis, and Fe-S cluster assembly. Transcription studies of the other fur homologue genes in the ⌬irrB strain indicated complementary functions of the Fur proteins in MSR-1. IrrB appears to be directly responsible for iron metabolism and homeostasis and to be indirectly involved in magnetosome formation. We propose two IrrB-regulated networks (under high-and low-iron conditions) in MSR-1 cells that control the balance of iron and oxygen metabolism and account for the coexistence of five Fur homologues. Iron is an essential nutrient for most organisms. It is involved in crucial biological processes such as nitrogen fixation, oxygen transport, central metabolism, respiration, gene regulation, and DNA biosynthesis (1). Under aerobic conditions at a neutral pH, iron is metabolically unavailable because of its insoluble state (2, 3). In cells, ferrous iron (Fe 2ϩ ) and ferric iron (Fe 3ϩ ) function, respectively, as the electron donor and electron acceptor, maintaining a compatible redox potential for many biochemical reactions (3). Excess ferrous iron catalyzes the formation of reactive oxygen species (ROS) via the Fenton reaction, resulting in cell damage or death (4). Bacteria and other microorganisms have developed various systems to maintain iron homeostasis, the most studied of which is the ferric uptake regulator (Fur) system. In Escherichia coli and Pseudomonas aeruginosa, iron binds Fur so as to occupy its promoter and inhibit the expression of Fur-controlled genes (5, 6).Magnetospirillum gryphiswaldense MSR-1, a Gram-negative alphaproteobacterium, is capable of synthesizing unique intracellular magnetic nanoparticles composed of Fe 3 O 4 , termed magnetosomes (7). The biosynthesis of magnetosomes, whose membranebound magnetite nanocrystals are aligned in chain-like s...

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Section: Discussionsupporting

confidence: 60%

Iron Response Regulator Protein IrrB in Magnetospirillum gryphiswaldense MSR-1 Helps Control the Iron/Oxygen Balance, Oxidative Stress Tolerance, and Magnetosome Formation

Wang

et al. 2015

Appl Environ Microbiol

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“…In addition to having variations in symbiosis (24, 39, 60), various members of the Bradyrhizobiaceae , including Bradyrhizobium , harbor diverse biochemical functions such as photosynthesis, nitrification, sulfur oxidation, aromatic degradation, and oligotrophy (22, 25, 26, 33, 34, 45, 56, 68, 70). Thus, a long-standing question is how the members of the Bradyrhizobiaceae have acquired these diverse biochemical features.…”

mentioning

confidence: 99%

Complete Genome Sequence of <i>Bradyrhizobium</i> sp. S23321: Insights into Symbiosis Evolution in Soil Oligotrophs

et al. 2012

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Bradyrhizobium sp. S23321 is an oligotrophic bacterium isolated from paddy field soil. Although S23321 is phylogenetically close to Bradyrhizobium japonicum USDA110, a legume symbiont, it is unable to induce root nodules in siratro, a legume often used for testing Nod factor-dependent nodulation. The genome of S23321 is a single circular chromosome, 7,231,841 bp in length, with an average GC content of 64.3%. The genome contains 6,898 potential protein-encoding genes, one set of rRNA genes, and 45 tRNA genes. Comparison of the genome structure between S23321 and USDA110 showed strong colinearity; however, the symbiosis islands present in USDA110 were absent in S23321, whose genome lacked a chaperonin gene cluster (groELS3) for symbiosis regulation found in USDA110. A comparison of sequences around the tRNA-Val gene strongly suggested that S23321 contains an ancestral-type genome that precedes the acquisition of a symbiosis island by horizontal gene transfer. Although S23321 contains a nif (nitrogen fixation) gene cluster, the organization, homology, and phylogeny of the genes in this cluster were more similar to those of photosynthetic bradyrhizobia ORS278 and BTAi1 than to those on the symbiosis island of USDA110. In addition, we found genes encoding a complete photosynthetic system, many ABC transporters for amino acids and oligopeptides, two types (polar and lateral) of flagella, multiple respiratory chains, and a system for lignin monomer catabolism in the S23321 genome. These features suggest that S23321 is able to adapt to a wide range of environments, probably including low-nutrient conditions, with multiple survival strategies in soil and rhizosphere.

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“…Analysis of the genome of 13 selected Rhizobiaceae strains revealed that the number of TBDT-like genes ranged from one in Mesorhizobium loti MAFF303099 to 14 in Azorhizobium caulinodans ORS571 (Lim 2010). The majority of the 54 rhizobial TBDTs identifi ed in that study are predicted to be involved in the uptake of iron-siderophore (26) or heme (13).…”

Section: Transporters For Metal Uptake Through the Outer Membranementioning

confidence: 95%