Identification of chromosomal alpha-proteobacterial small RNAs by comparative genome analysis and detection in Sinorhizobium meliloti strain 1021

Ulvé, Vincent; Sevin, Emeric W; Chéron, Angélique; Barloy-Hubler, Frédérique

doi:10.1186/1471-2164-8-467

Cited by 54 publications

(72 citation statements)

References 80 publications

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“…The same pattern of induction was observed in strain Smbl503 (complemented hfq mutant) (data not shown). Further experiments will be required to elucidate whether S. meliloti Hfq auto-controls its own expression at a translational level, as described for E. coli (65). The greater expression level of hfq during stationary phase suggests that Hfq plays a role in the stationary phase adaptation and may account, at least in part, for the lower cell density reached by the mutant than by the parental strain.…”

Section: Resultsmentioning

confidence: 99%

“…Such a regulatory strategy would allow the bacteria to react quickly and at lower energetic cost to the stresses and sudden variations in their environments that they experience during the establishment of the symbiosis (39); as recently reviewed by Waters and Storz (69), sRNA-mediated regulation has several advantages compared to protein-regulated regulation during stress responses. Recent comparative genome analysis and prediction studies have suggested the existence of a number of sRNAs in S. meliloti, and some have been experimentally verified (11,65,68), but their regulatory roles in bacterial physiology and symbiosis has not yet been investigated. Expression of several of these predicted sRNAs in S. meliloti has been confirmed by Northern blots and microarray analysis.…”

Section: Discussionmentioning

confidence: 99%

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The Sinorhizobium meliloti RNA Chaperone Hfq Mediates Symbiosis of S. meliloti and Alfalfa

et al. 2010

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There exist commonalities between symbiotic Sinorhizobium meliloti and pathogenic Brucella bacteria in terms of extensive gene synteny and the requirements for intracellular survival in their respective hosts. The RNA chaperone Hfq is essential for virulence for several bacterial groups, including Brucella; however, its role in S. meliloti has not been investigated. Our studies of an S. meliloti loss-of-function hfq mutant have revealed that Hfq plays a key role in the establishment of the symbiosis between S. meliloti and its host Medicago sativa. S. meliloti Hfq is involved in controlling the population density under a free-living state and affects the growth parameters and nodulation. An hfq mutant poorly colonizes the infection threads that are necessary for the bacteria to invade the developing nodule. An hfq mutant is severely impaired in its ability to invade plant cells within the nodule, which leads to the formation of small, ineffective nodules unable to fix nitrogen. In culture, the hfq mutant did not accumulate transcripts of nifA, which encodes a key regulator necessary for nitrogen fixation. Hfq may be involved in regulation of several proteins relevant to hfq mutant phenotypes. The crucial role of Hfq in symbiosis suggests that small regulatory RNAs are important for its interactions with its plant host.The alpha subgroup of proteobacteria includes members such as Sinorhizobium meliloti, which establishes a symbiosis with certain leguminous plants, as well as members, such as Brucella abortus, that are highly pathogenic to animals and humans. Despite the very different outcomes of the chronic intracellular infections established by S. meliloti and B. abortus in their respective hosts, parallels can be drawn because in both cases the bacteria need to survive within acidic membrane compartments for a prolonged time after endocytosis (50). Comparisons of genomic sequences between brucellae and rhizobia have revealed similarities. For example, extensive gene synteny exists between chromosome I of Brucella and the genome of Mesorhizobium loti, while chromosome II shares regions of gene synteny with the pSym megaplasmids of S. meliloti. In addition, the transport and metabolic capabilities of Brucella have similarities to those of the plant symbiont (46). Genomic comparisons suggest that these two types of bacteria share a complex evolutionary history and that Brucella evolved from soil/plant-associated ancestral bacteria of the Rhizobium/ Agrobacterium group (46).The parallel between these two bacterial groups is well illustrated by the inner membrane protein BacA, which is critical for the maintenance of the chronic intracellular infections that underlie these two very diverse host-bacterial relationships (20, 35). S. meliloti bacA mutants lyse soon after being endocytosed into the plant cytoplasm (20), while B. abortus bacA mutants are defective in intracellular replication in macrophages and are unable to establish a chronic infection in BALB/c mice (35). BacA is required for the transport of certai...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The Sinorhizobium meliloti RNA Chaperone Hfq Mediates Symbiosis of S. meliloti and Alfalfa

et al. 2010

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“…In recent years, comparative genomics-based predictions have become a standard method to search for ncRNA genes conserved in at least two bacterial genomes (10,53,100,163,210,303,309). Thus, the high number of genome sequences from marine picocyanobacteria provides an excellent data set for the computational prediction of ncRNA genes.…”

Section: Two-component Systems and Crp-type Regulatorsmentioning

confidence: 99%

Ecological Genomics of Marine Picocyanobacteria

Scanlan

Ostrowski

Mazard

et al. 2009

Microbiol Mol Biol Rev

657

824

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SUMMARY Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus numerically dominate the picophytoplankton of the world ocean, making a key contribution to global primary production. Prochlorococcus was isolated around 20 years ago and is probably the most abundant photosynthetic organism on Earth. The genus comprises specific ecotypes which are phylogenetically distinct and differ markedly in their photophysiology, allowing growth over a broad range of light and nutrient conditions within the 45°N to 40°S latitudinal belt that they occupy. Synechococcus and Prochlorococcus are closely related, together forming a discrete picophytoplankton clade, but are distinguishable by their possession of dissimilar light-harvesting apparatuses and differences in cell size and elemental composition. Synechococcus strains have a ubiquitous oceanic distribution compared to that of Prochlorococcus strains and are characterized by phylogenetically discrete lineages with a wide range of pigmentation. In this review, we put our current knowledge of marine picocyanobacterial genomics into an environmental context and present previously unpublished genomic information arising from extensive genomic comparisons in order to provide insights into the adaptations of these marine microbes to their environment and how they are reflected at the genomic level.

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“…The mass spectrometric analysis of the samples was performed with an Orbitrap Velos Pro mass spectrometer (Thermo Scientific, Germany). An Ultimate nanoscale rapid-separation LC-high-pressure liquid chromatography (nanoRSLC-HPLC) system (Thermo Scientific, Germany), equipped with a custom 20-cm by 75-m column filled with 1.7-m C 18 beads, was connected on line to the mass spectrometer through a Thermo Scientific Nanospray Flex ion source. One microliter of the tryptic digest was injected onto a C 18 micro-preconcentration column (300 m [inner diameter] by 5 mm).…”

Section: Methodsmentioning

confidence: 99%

“…meliloti has been shown to express more than 400 different sRNAs under different growth conditions and lifestyles, i.e., both free-living in the soil and symbiotically associated in a plant (15)(16)(17)(18)(19)(20)(21). In addition, S. meliloti expresses a functional homolog of the Escherichia coli Hfq protein, a chaperone of RNA-RNA interactions and a modulator of RNA activity (22)(23)(24)(25)(26)(27)(28)(29).…”

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confidence: 99%

Regulation of Polyhydroxybutyrate Accumulation in Sinorhizobium meliloti by the Trans -Encoded Small RNA MmgR

et al. 2017

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Riboregulation has a major role in the fine-tuning of multiple bacterial processes. Among the RNA players, trans-encoded untranslated small RNAs (sRNAs) regulate complex metabolic networks by tuning expression from multiple target genes in response to numerous signals. In Sinorhizobium meliloti, over 400 sRNAs are expressed under different stimuli. The sRNA MmgR (standing for Makes more granules Regulator) has been of particular interest to us since its sequence and structure are highly conserved among the alphaproteobacteria and its expression is regulated by the amount and quality of the bacterium's available nitrogen source. In this work, we explored the biological role of MmgR in S. meliloti 2011 by characterizing the effect of a deletion of the internal conserved core of mmgR (mmgR Δ33-51 ). This mutation resulted in larger amounts of polyhydroxybutyrate (PHB) distributed into more intracellular granules than are found in the wild-type strain. This phenotype was expressed upon cessation of balanced growth owing to nitrogen depletion in the presence of surplus carbon (i.e., at a carbon/nitrogen molar ratio greater than 10). The normal PHB accumulation was complemented with a wild-type mmgR copy but not with unrelated sRNA genes. Furthermore, the expression of mmgR limited PHB accumulation in the wild type, regardless of the magnitude of the C surplus. Quantitative proteomic profiling and quantitative reverse transcription-PCR (qRT-PCR) revealed that the absence of MmgR results in a posttranscriptional overexpression of both PHB phasin proteins (PhaP1 and PhaP2). Together, our results indicate that the widely conserved alphaproteobacterial MmgR sRNA fine-tunes the regulation of PHB storage in S. meliloti. IMPORTANCE High-throughput RNA sequencing has recently uncovered an overwhelming number of trans-encoded small RNAs (sRNAs) in diverse prokaryotes. In the nitrogen-fixing alphaproteobacterial symbiont of alfalfa root nodules Sinorhizobium meliloti, only four out of hundreds of identified sRNA genes have been functionally characterized. Thus, uncovering the biological role of sRNAs currently represents a major issue and one that is particularly challenging because of the usually subtle quantitative regulation contributed by most characterized sRNAs. Here, we have characterized the function of the broadly conserved alphaproteobacterial sRNA gene mmgR in S. meliloti. Our results strongly suggest that mmgR encodes a negative regulator of the accumulation of polyhydroxybutyrate, the major carbon and reducing power storage polymer in S. meliloti cells growing under conditions of C/N overbalance.

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Identification of chromosomal alpha-proteobacterial small RNAs by comparative genome analysis and detection in Sinorhizobium meliloti strain 1021

Cited by 54 publications

References 80 publications

The Sinorhizobium meliloti RNA Chaperone Hfq Mediates Symbiosis of S. meliloti and Alfalfa

The Sinorhizobium meliloti RNA Chaperone Hfq Mediates Symbiosis of S. meliloti and Alfalfa

Ecological Genomics of Marine Picocyanobacteria

Regulation of Polyhydroxybutyrate Accumulation in Sinorhizobium meliloti by the Trans -Encoded Small RNA MmgR

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