Versatile roles of the chaperonin GroEL in microorganism-insect interactions

Kupper, Maria; Gupta, Shishir; Feldhaar, Heike; Gross, Roy

doi:10.1111/1574-6968.12390

Cited by 61 publications

(56 citation statements)

References 98 publications

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“…This mutation-driven bias generally favors A+T nucleotides and has extreme effects on polypeptide composition; all encoded proteins in most insect symbionts are strongly shifted toward amino acids that enable higher A+T in the DNA sequence. The negative effects of these mutations are partially masked by constitutively high expression of chaperones that help to stabilize impaired proteins (66)(67)(68), but high chaperone expression is itself metabolically costly.…”

Section: Increased Genetic Incompatabilitymentioning

confidence: 99%

“…The major effect of deleterious amino acid replacements is to lower protein stability. As a general compensation for protein instability, chaperone expression in obligate symbionts is high even under nonstress conditions (68). In Buchnera, chaperonin (GroEL) is produced constitutively at levels equivalent to those during extreme heat shock in Escherichia coli (66).…”

Section: Consequences Of Symbiosis For Host Evolutionmentioning

confidence: 99%

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Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

Bennett

Moran

2015

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

443

515

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Many eukaryotes have obligate associations with microorganisms that are transmitted directly between generations. A model for heritable symbiosis is the association of aphids, a clade of sapfeeding insects, and Buchnera aphidicola, a gammaproteobacterium that colonized an aphid ancestor 150 million years ago and persists in almost all 5,000 aphid species. Symbiont acquisition enables evolutionary and ecological expansion; aphids are one of many insect groups that would not exist without heritable symbiosis. Receiving less attention are potential negative ramifications of symbiotic alliances. In the short run, symbionts impose metabolic costs. Over evolutionary time, hosts evolve dependence beyond the original benefits of the symbiosis. Symbiotic partners enter into an evolutionary spiral that leads to irreversible codependence and associated risks. Host adaptations to symbiosis (e.g., immune-system modification) may impose vulnerabilities. Symbiont genomes also continuously accumulate deleterious mutations, limiting their beneficial contributions and environmental tolerance. Finally, the fitness interests of obligate heritable symbionts are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the host-symbiont interface are predicted to follow a coevolutionary arms race, as observed for genes governing host-pathogen interactions. On the macroevolutionary scale, the rapid evolution of interacting symbiont and host genes is predicted to accelerate host speciation rates by generating genetic incompatibilities. However, degeneration of symbiont genomes may ultimately limit the ecological range of host species, potentially increasing extinction risk. Recent results for the aphidBuchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.Buchnera | aphid | Muller's ratchet | selection levels | coevolution

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Section: Increased Genetic Incompatabilitymentioning

confidence: 99%

Section: Consequences Of Symbiosis For Host Evolutionmentioning

confidence: 99%

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

Bennett

Moran

2015

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

443

515

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“…Moreover, GroEL is also an essential symbiosis factor in the insects required for endosymbionts maintenance or counteracting the negative effects of deleterious mutations arising from genome erosion (26). Far Western blotting experiments revealed interaction of ColA with GroEL and proposed to be involved in cell elongation of the endosymbiont (23).…”

Section: Ncr247-ribosomal Protein Interactions: Modulation Of the Bacmentioning

confidence: 99%

Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms

Farkas

Maróti

Dürgő

et al. 2014

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

154

178

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Symbiosis between rhizobia soil bacteria and legume plants results in the formation of root nodules where plant cells are fully packed with nitrogen fixing bacteria. In the host cells, the bacteria adapt to the intracellular environment and gain the ability for nitrogen fixation. Depending on the host plants, the symbiotic fate of bacteria can be either reversible or irreversible. In Medicago and related legume species, the bacteria undergo a host-directed multistep differentiation process culminating in the formation of elongated and branched polyploid bacteria with definitive loss of cell division ability. The plant factors are nodule-specific symbiotic peptides. Approximately 600 of them are nodule-specific cysteine-rich (NCR) peptides produced in the rhizobium-infected plant cells. NCRs are targeted to the endosymbionts, and concerted action of different sets of peptides governs different stages of endosymbiont maturation, whereas the symbiotic function of individual NCRs is unknown. This study focused on NCR247, a cationic peptide exhibiting in vitro antimicrobial activities. We show that NCR247 acts in those nodule cells where bacterial cell division is arrested and cell elongation begins. NCR247 penetrates the bacteria and forms complexes with many bacterial proteins. Interaction with FtsZ required for septum formation is one of the host interventions for inhibiting bacterial cell division. Complex formation with the ribosomal proteins affects translation and contributes to altered proteome and physiology of the endosymbiont. Binding to the chaperone GroEL amplifies the NCR247-modulated biological processes. We show that GroEL1 of Sinorhizobium meliloti is required for efficient infection, terminal differentiation, and nitrogen fixation.bacterial targets | antimicrobial peptides | protein interactions | translation inhibition | host peptides S ymbiosis between microbes and hosts, like legumes and various insects, often results in the formation of symbiotic organs where host cells harbor thousands of endosymbiotic bacteria. In rhizobium-legume symbiosis, rhizobia in the soil interact with their host legume and induce the formation of root nodules where bacteria reside in the host cytosol in membrane-enclosed vesicles called symbiosomes. The bacteria adapt to the endosymbiotic lifestyle in the plant cells and gain the capacity for nitrogen fixation, thereby ensuring the nitrogen need of the host plant.In addition to the physiological changes required for nitrogen fixation, in certain rhizobium-legume interactions, like in the Medicago truncatula-Sinorhizobium meliloti symbiosis, the bacteria undergo an additional remarkable differentiation process (1). The endosymbiotic bacteria called bacteroids become polyploid, noncultivable elongated, and frequently branched cells (2). This terminal bacterial differentiation is provoked by hundreds of nodule-specific cysteine-rich (NCR) host peptides that are exclusively expressed in the rhizobium-infected symbiotic cells (3).Nodule development and bacterial infection a...

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“…GroEL and GroHps are the most abundant proteins produced by bacteria (Baumann et al, 1996;Kupper et al, 2014). The groel gene is highly conserved in primary endosymbionts (Kupper et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

A novel groel gene from the endosymbiont of beet leafhopper, Candidatus Sulcia muelleri

Nusayr¹,

Creamer²

2017

Afr. J. Microbiol. Res.

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Curtoviruses are transmitted by the beet leafhopper Circulifer tenellus, in a circulative (nonpropagative) manner. Curtoviruses are phloem-limited and are acquired by the vector during feeding. Sap-feeding insects harbor endosymbionts which can help provide essential nutrients required for the insects' survival. Candidatus Sulcia muelleri is an endosymbiont present in the beet leafhopper identified during this study. A housekeeping gene, groel, was identified from the endosymbiont. The groel gene sequence from this strain of Ca. S. muelleri differs from all other strains published in NCBI, suggesting the presence of a new strain, which was named S. muelleri beet leafhopper (SMBLH). A GroEL-homolog protein produced from groel was found in different vectors with circulative transmission. Analysis of nucleotide and translated sequences, using alignment, phylogenetic trees, and predicted secondary and tertiary structures showed that SMBLH GroHp has similarities to Escherichia coli GroEL and the GroEL-homolog proteins from Hamiltonella and Buchnera, endosymbionts of whiteflies and aphids, respectively. GroHp and GroEL were expressed as fusion proteins. Electron microscopy analyses indicate that purified expressed GroHp and GroEL proteins demonstrate correct folding.

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Versatile roles of the chaperonin GroEL in microorganism-insect interactions

Cited by 61 publications

References 98 publications

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms

A novel groel gene from the endosymbiont of beet leafhopper, Candidatus Sulcia muelleri

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