Sensing, Signaling, and Secretion: A Review and Analysis of Systems for Regulating Host Interaction in Wolbachia
Abstract
:1. Introduction to Wolbachia
2. How do Other Bacteria Interface with Their Environment?
3. Materials and Methods
4. Sensing and Signaling
5. Transcriptional Regulation
6. Secretion Systems
7. When do Wolbachia Respond to Their Environment?
8. Future Directions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Dumler, J.S.; Barbet, A.F.; Bekker, C.; Dasch, G.A.; Palmer, G.H.; Ray, S.C.; Rikihisa, Y.; Rurangirwa, F.R. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and’HGE agent’as subjective synonyms of Ehrlichia phagocytophila. Int. J. Syst. Evol. Microbiol. 2001, 51, 2145–2165. [Google Scholar] [PubMed] [Green Version]
- Muñoz-Gómez, S.A.; Hess, S.; Burger, G.; Lang, B.F.; Susko, E.; Slamovits, C.H.; Roger, A.J. An updated phylogeny of the Alphaproteobacteria reveals that the parasitic Rickettsiales and Holosporales have independent origins. Elife 2019, 8, e42535. [Google Scholar] [CrossRef] [PubMed]
- Epis, S.; Mandrioli, M.; Genchi, M.; Montagna, M.; Sacchi, L.; Pistone, D.; Sassera, D. Localization of the bacterial symbiont Candidatus Midichloria mitochondrii within the hard tick Ixodes ricinus by whole-mount FISH staining. Ticks and Tick-Borne Diseases 2013, 4, 39–45. [Google Scholar] [CrossRef] [PubMed]
- Werren, J.H.; Baldo, L.; Clark, M.E. Wolbachia: Master manipulators of invertebrate biology. Nat. Rev. Micro. 2008, 6, 741–751. [Google Scholar] [CrossRef] [PubMed]
- Stouthamer, R.; Breeuwer, J.A.J.; Hurst, G.D.D. Wolbachia pipientis: Microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 1999, 53, 71–102. [Google Scholar] [CrossRef]
- Min, K.-T.; Benzer, S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl. Acad. Sci. USA 1997, 94, 10792–10796. [Google Scholar] [CrossRef] [Green Version]
- Zug, R.; Hammerstein, P. Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biological Reviews 2015, 90, 89–111. [Google Scholar] [CrossRef]
- Weeks, A.R.; Turelli, M.; Harcombe, W.R.; Reynolds, K.T.; Hoffmann, A.A. From parasite to mutualist: Rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 2007, 5, e114. [Google Scholar] [CrossRef] [Green Version]
- Hertig, M. The Rickettsia, Wolbachia pipientis (gen. et sp.n.) and Associated Inclusions of the Mosquito, Culex pipiens. Parasitology 1936, 28, 453–486. [Google Scholar] [CrossRef]
- Hertig, M.; Wolbach, S.B. Studies on rickettsia-like micro-organisms in insects. The J. Med. Res. 1924, 44, 329. [Google Scholar]
- Werren, J.H.; Zhang, W.; Guo, L.R. Evolution and phylogeny of Wolbachia—reproductive parasites of arthropods. Proc. R. Soc. Lond. B 1995, 261, 55–63. [Google Scholar]
- Bensaadi–Merchermek, N.; Salvado, J.-C.; Cagnon, C.; Karama, S.; Mouchès, C. Characterization of the unlinked 16S rDNA and 23S-5S rRNA operon of Wolbachia pipientis, a prokaryotic parasite of insect gonads. Gene 1995, 165, 81–86. [Google Scholar] [CrossRef]
- Hamm, C.A.; Begun, D.J.; Vo, A.; Smith, C.C.; Saelao, P.; Shaver, A.O.; Jaenike, J.; Turelli, M. Wolbachia do not live by reproductive manipulation alone: Infection polymorphism in Drosophila suzukii and D. subpulchrella. Mol. Ecol. 2014, 23, 4871–4885. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kriesner, P.; Hoffmann, A.A. Rapid spread of a Wolbachia infection that does not affect host reproduction in Drosophila simulans cage populations. Evolution 2018, 72, 1475–1487. [Google Scholar] [CrossRef]
- Turelli, M.; Cooper, B.S.; Richardson, K.M.; Ginsberg, P.S.; Peckenpaugh, B.; Antelope, C.X.; Kim, K.J.; May, M.R.; Abrieux, A.; Wilson, D.A. Rapid global spread of wRi-like Wolbachia across multiple Drosophila. Curr. Biol. 2018, 28, 963–971.e968. [Google Scholar] [CrossRef] [Green Version]
- Zug, R.; Hammerstein, P. Still a host of hosts for Wolbachia: Analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE 2012, 7. [Google Scholar] [CrossRef] [Green Version]
- Weinert, L.A.; Araujo-Jnr, E.V.; Ahmed, M.Z.; Welch, J.J. The incidence of bacterial endosymbionts in terrestrial arthropods. Proc. R. Soc. Lond. B 2015, 282, 20150249. [Google Scholar] [CrossRef]
- Newton, I.L.; Rice, D.W. The Jekyll and Hyde symbiont: Could Wolbachia be a nutritional mutualist? J. Bacteriol. 2020, 202. [Google Scholar] [CrossRef]
- Teixeira, L.; Ferreira, Á.; Ashburner, M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 2008, 6, e1000002. [Google Scholar] [CrossRef] [Green Version]
- Raychoudhury, R.; Baldo, L.; Oliveira, D.C.S.G.; Werren, J.H. Modes of acquisition of Wolbachia: Horizontal transfer, hybrid introgression, and codivergence in the Nasonia species complex. Evolution 2009, 63, 165–183. [Google Scholar] [CrossRef]
- Conner, W.R.; Blaxter, M.L.; Anfora, G.; Ometto, L.; Rota-Stabelli, O.; Turelli, M. Genome comparisons indicate recent transfer of wRi-like Wolbachia between sister species Drosophila suzukii and D. subpulchrella. Ecol. Evol. 2017. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, X.; Lindsey, A.R.I.; Chatterjee, P.; Werren, J.H.; Stouthamer, R.; Yi, S.V. Distinct epigenomic and transcriptomic modifications associated with Wolbachia-mediated asexuality. PLoS Path. 2020, 16, e1008397. [Google Scholar] [CrossRef] [PubMed]
- Bailly-Bechet, M.; Martins-Simões, P.; Szöllősi, G.J.; Mialdea, G.; Sagot, M.-F.; Charlat, S. How long does Wolbachia remain on board? Mol. Biol. Evol. 2017, 34, 1183–1193. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, M.; Sun, L.V.; Vamathevan, J.; Riegler, M.; Deboy, R.; Brownlie, J.C.; McGraw, E.A.; Martin, W.; Esser, C.; Ahmadinejad, N.; et al. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: A streamlined genome overrun by mobile genetic elements. PLoS Biol. 2004, 2, 327–341. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoffmann, A.A.; Ross, P.A.; Rasic, G. Wolbachia strains for disease control: Ecological and evolutionary considerations. Ecol. Evol. 2015, 8, 751–768. [Google Scholar]
- Schmidt, T.L.; Barton, N.H.; Rašić, G.; Turley, A.P.; Montgomery, B.L.; Iturbe-Ormaetxe, I.; Cook, P.E.; Ryan, P.A.; Ritchie, S.A.; Hoffmann, A.A. Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti. PLoS Biol. 2017, 15, e2001894. [Google Scholar] [CrossRef]
- Dutra, H.L.C.; Rocha, M.N.; Dias, F.B.S.; Mansur, S.B.; Caragata, E.P.; Moreira, L.A. Wolbachia blocks currently circulating Zika virus isolates in Brazilian Aedes aegypti mosquitoes. Cell Host & Microbe 2016, 19, 771–774. [Google Scholar]
- Lindsey, A.R.I.; Bhattacharya, T.; Newton, I.L.G.; Hardy, R.W. Conflict in the intracellular lives of endosymbionts and viruses: A mechanistic look at Wolbachia—mediated pathogen-blocking. Viruses 2018, 10, 141. [Google Scholar] [CrossRef] [Green Version]
- Hedges, L.M.; Brownlie, J.C.; O’neill, S.L.; Johnson, K.N. Wolbachia and virus protection in insects. Science 2008, 322, 702. [Google Scholar] [CrossRef]
- Moreira, L.A.; Iturbe-Ormaetxe, I.; Jeffery, J.A.; Lu, G.; Pyke, A.T.; Hedges, L.M.; Rocha, B.C.; Hall-Mendelin, S.; Day, A.; Riegler, M.; et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium. Cell 2009, 139, 1268–1278. [Google Scholar] [CrossRef] [Green Version]
- White, P.M.; Serbus, L.R.; Debec, A.; Codina, A.; Bray, W.; Guichet, A.; Lokey, R.S.; Sullivan, W. Reliance of Wolbachia on high rates of host proteolysis revealed by a genome-wide RNAi screen of Drosophila cells. Genetics 2017, 205, 1473–1488. [Google Scholar] [CrossRef] [Green Version]
- Grobler, Y.; Yun, C.Y.; Kahler, D.J.; Bergman, C.M.; Lee, H.; Oliver, B.; Lehmann, R. Whole genome screen reveals a novel relationship between Wolbachia levels and Drosophila host translation. PLoS Path. 2018, 14, e1007445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Newton, I.L.; Savytskyy, O.; Sheehan, K.B. Wolbachia utilize host actin for efficient maternal transmission in Drosophila melanogaster. PLoS Path. 2015, 11, e1004798. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chrostek, E.; Teixeira, L. Mutualism breakdown by amplification of Wolbachia genes. PLoS Biol. 2015, 13, e1002065. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- LePage, D.P.; Metcalf, J.A.; Bordenstein, S.R.; On, J.; Perlmutter, J.I.; Shropshire, J.D.; Layton, E.M.; Funkhouser-Jones, L.J.; Beckmann, J.F.; Bordenstein, S.R. Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature 2017, 543, 243–247. [Google Scholar] [CrossRef] [Green Version]
- Beckmann, J.F.; Ronau, J.A.; Hochstrasser, M. A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat. Micro. 2017, 2, 17007. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.; Ronau, J.A.; Beckmann, J.F.; Hochstrasser, M. A Wolbachia nuclease and its binding partner provide a distinct mechanism for cytoplasmic incompatibility. Proc. Natl. Acad. Sci. USA 2019, 116, 22314–22321. [Google Scholar] [CrossRef]
- Rice, D.W.; Sheehan, K.B.; Newton, I.L. Large–scale identification of Wolbachia pipientis effectors. Genome Biol. Evol. 2017, 9, 1925–1937. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sheehan, K.B.; Martin, M.; Lesser, C.F.; Isberg, R.R.; Newton, I.L. Identification and characterization of a candidate Wolbachia pipientis type IV effector that interacts with the actin cytoskeleton. mBio 2016, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Newton, I.L.; Sheehan, K.B. Gateway entry vector library of Wolbachia pipientis candidate effectors from strain wMel. Microbiol. Resour. Announc. 2018, 7, e00806–00818. [Google Scholar] [CrossRef] [Green Version]
- Perlmutter, J.I.; Bordenstein, S.R.; Unckless, R.L.; LePage, D.P.; Metcalf, J.A.; Hill, T.; Martinez, J.; Jiggins, F.M.; Bordenstein, S.R. The phage gene wmk is a candidate for male killing by a bacterial endosymbiont. PLoS Path. 2019, 15. [Google Scholar] [CrossRef]
- Bordenstein, S.R.; Bordenstein, S.R. Eukaryotic association module in phage WO genomes from Wolbachia. Nat. Commun. 2016, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miravet-Verde, S.; Lloréns-Rico, V.; Serrano, L. Alternative transcriptional regulation in genome-reduced bacteria. Curr. Opin. Microbiol. 2017, 39, 89–95. [Google Scholar] [CrossRef] [PubMed]
- Hansen, A.K.; Degnan, P.H. Widespread expression of conserved small RNAs in small symbiont genomes. ISME J. 2014, 8, 2490–2502. [Google Scholar] [CrossRef] [PubMed]
- Fenn, K.; Blaxter, M. Wolbachia genomes: Revealing the biology of parasitism and mutualism. Trends Parasitol. 2006, 22, 60–65. [Google Scholar] [CrossRef] [PubMed]
- Lindsey, A.R.I.; Werren, J.H.; Richards, S.; Stouthamer, R. Comparative genomics of a parthenogenesis–inducing Wolbachia symbiont. G3: Genes|Genomes|Genetics 2016, 6, 2113–2123. [Google Scholar] [CrossRef]
- Dorman, C.J.; McKenna, S.; Beloin, C. Regulation of virulence gene expression in Shigella flexneri, a facultative intracellular pathogen. Int. J. Med. Microbiol. 2001, 291, 89–96. [Google Scholar] [CrossRef]
- Gorvel, J.P.; Moreno, E. Brucella intracellular life: From invasion to intracellular replication. Vet. Microbiol. 2002, 90, 281–297. [Google Scholar] [CrossRef]
- Sjöstedt, A. Intracellular survival mechanisms of Francisella tularensis, a stealth pathogen. Microb. Infect. 2006, 8, 561–567. [Google Scholar] [CrossRef]
- Rohde, K.H.; Abramovitch, R.B.; Russell, D.G. Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host & Microbe 2007, 2, 352–364. [Google Scholar]
- Ibarra, J.A.; Steele-Mortimer, O. Salmonella-the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell. Microbiol. 2009, 11, 1579–1586. [Google Scholar] [PubMed] [Green Version]
- Molmeret, M.; Bitar, D.M.; Han, L.; Kwaik, Y.A. Cell biology of the intracellular infection by Legionella pneumophila. Microb. Infect. 2004, 6, 129–139. [Google Scholar] [CrossRef]
- Haselkorn, T.S. The Spiroplasma heritable bacterial endosymbiont of Drosophila. Fly 2010, 4, 80–87. [Google Scholar] [CrossRef] [Green Version]
- Van Schaik, E.J.; Chen, C.; Mertens, K.; Weber, M.M.; Samuel, J.E. Molecular pathogenesis of the obligate intracellular bacterium Coxiella burnetii. Nat. Rev. Micro. 2013, 11, 561–573. [Google Scholar] [CrossRef] [Green Version]
- Wyrick, P.B. Intracellular survival by Chlamydia: Microreview. Cell. Microbiol. 2000, 2, 275–282. [Google Scholar] [CrossRef]
- Persat, A.; Nadell, C.D.; Kim, M.K.; Ingremeau, F.; Siryaporn, A.; Drescher, K.; Wingreen, N.S.; Bassler, B.L.; Gitai, Z.; Stone, H.A. The mechanical world of bacteria. Cell 2015, 161, 988–997. [Google Scholar] [CrossRef] [Green Version]
- Kotte, O.; Zaugg, J.B.; Heinemann, M. Bacterial adaptation through distributed sensing of metabolic fluxes. Mol. Syst. Biol. 2010, 6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galperin, M.Y. A census of membrane-bound and intracellular signal transduction proteins in bacteria: Bacterial IQ, extroverts and introverts. BMC Microbiol. 2005, 5, 35. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marijuán, P.C.; Navarro, J.; del Moral, R. How prokaryotes ‘encode’their environment: Systemic tools for organizing the information flow. BioSyst. 2018, 164, 26–38. [Google Scholar] [CrossRef]
- Marijuán, P.C.; Navarro, J.; del Moral, R. On prokaryotic intelligence: Strategies for sensing the environment. BioSyst. 2010, 99, 94–103. [Google Scholar] [CrossRef]
- Gao, R.; Mack, T.R.; Stock, A.M. Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem. Sci. 2007, 32, 225–234. [Google Scholar] [CrossRef] [Green Version]
- Capra, E.J.; Laub, M.T. Evolution of two-component signal transduction systems. Annu. Rev. Microbiol. 2012, 66, 325–347. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Podgornaia, A.I.; Laub, M.T. Determinants of specificity in two-component signal transduction. Curr. Opin. Microbiol. 2013, 16, 156–162. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McPhee, J.B.; Lewenza, S.; Hancock, R.E. Cationic antimicrobial peptides activate a two-component regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol. Microbiol. 2003, 50, 205–217. [Google Scholar] [CrossRef] [PubMed]
- Beier, D.; Gross, R. Regulation of bacterial virulence by two–component systems. Curr. Opin. Microbiol. 2006, 9, 143–152. [Google Scholar] [CrossRef] [PubMed]
- Walters, S.B.; Dubnau, E.; Kolesnikova, I.; Laval, F.; Daffe, M.; Smith, I. The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol. Microbiol. 2006, 60, 312–330. [Google Scholar] [CrossRef]
- Nikaido, H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 2003, 67, 593–656. [Google Scholar] [CrossRef] [Green Version]
- Batut, J.; Andersson, S.G.; O’Callaghan, D. The evolution of chronic infection strategies in the α-proteobacteria. Nat. Rev. Micro. 2004, 2, 933–945. [Google Scholar] [CrossRef]
- Martínez-Núñez, C.; Altamirano-Silva, P.; Alvarado-Guillén, F.; Moreno, E.; Guzmán-Verri, C.; Chaves-Olarte, E. The two-component system BvrR/BvrS regulates the expression of the type IV secretion system VirB in Brucella abortus. J. Bacteriol. 2010, 192, 5603–5608. [Google Scholar] [CrossRef] [Green Version]
- Cheng, Z.; Wang, X.; Rikihisa, Y. Regulation of type IV secretion apparatus genes during Ehrlichia chaffeensis intracellular development by a previously unidentified protein. J. Bacteriol. 2008, 190, 2096–2105. [Google Scholar] [CrossRef] [Green Version]
- Li, Z.; Carlow, C.K. Characterization of transcription factors that regulate the type IV secretion system and riboflavin biosynthesis in Wolbachia of Brugia malayi. PLoS ONE 2012, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Altman, E.; Segal, G. The response regulator CpxR directly regulates expression of several Legionella pneumophila icm/dot components as well as new translocated substrates. J. Bacteriol. 2008, 190, 1985–1996. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zusman, T.; Aloni, G.; Halperin, E.; Kotzer, H.; Degtyar, E.; Feldman, M.; Segal, G. The response regulator PmrA is a major regulator of the icm/dot type IV secretion system in Legionella pneumophila and Coxiella burnetii. Mol. Microbiol. 2007, 63, 1508–1523. [Google Scholar] [CrossRef] [PubMed]
- Büttner, D. Protein export according to schedule: Architecture, assembly, and regulation of type III secretion systems from plant-and animal-pathogenic bacteria. Microbiol. Mol. Biol. Rev. 2012, 76, 262–310. [Google Scholar] [CrossRef] [Green Version]
- Grohmann, E.; Christie, P.J.; Waksman, G.; Backert, S. Type IV secretion in Gram-negative and Gram-positive bacteria. Mol. Microbiol. 2018, 107, 455–471. [Google Scholar] [CrossRef]
- Cascales, E.; Christie, P.J. Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 2004, 304, 1170–1173. [Google Scholar] [CrossRef] [Green Version]
- Alvarez-Martinez, C.E.; Christie, P.J. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 2009, 73, 775–808. [Google Scholar] [CrossRef] [Green Version]
- Mougous, J.D.; Cuff, M.E.; Raunser, S.; Shen, A.; Zhou, M.; Gifford, C.A.; Goodman, A.L.; Joachimiak, G.; Ordoñez, C.L.; Lory, S. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 2006, 312, 1526–1530. [Google Scholar] [CrossRef] [Green Version]
- Pukatzki, S.; Ma, A.T.; Sturtevant, D.; Krastins, B.; Sarracino, D.; Nelson, W.C.; Heidelberg, J.F.; Mekalanos, J.J. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. USA 2006, 103, 1528–1533. [Google Scholar] [CrossRef] [Green Version]
- Leiman, P.G.; Basler, M.; Ramagopal, U.A.; Bonanno, J.B.; Sauder, J.M.; Pukatzki, S.; Burley, S.K.; Almo, S.C.; Mekalanos, J.J. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. USA 2009, 106, 4154–4159. [Google Scholar] [CrossRef] [Green Version]
- Kanonenberg, K.; Spitz, O.; Erenburg, I.N.; Beer, T.; Schmitt, L. Type I secretion system—it takes three and a substrate. FEMS Microbiol. Lett. 2018, 365, fny094. [Google Scholar] [CrossRef] [PubMed]
- Radics, J.; Königsmaier, L.; Marlovits, T.C. Structure of a pathogenic type 3 secretion system in action. Nat. Struct. Mol. Biol. 2014, 21, 82–87. [Google Scholar] [CrossRef]
- Korotkov, K.V.; Sandkvist, M.; Hol, W.G. The type II secretion system: Biogenesis, molecular architecture and mechanism. Nat. Rev. Micro. 2012, 10, 336–351. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leo, J.C.; Grin, I.; Linke, D. Type V secretion: Mechanism (s) of autotransport through the bacterial outer membrane. Philos. Trans. R. Soc. B Biol. Sci. 2012, 367, 1088–1101. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cho, K.-O.; Kim, G.-W.; Lee, O.-K. Wolbachia bacteria reside in host Golgi–related vesicles whose position is regulated by polarity proteins. PLoS ONE 2011, 6, e22703. [Google Scholar] [CrossRef] [Green Version]
- Kudva, R.; Denks, K.; Kuhn, P.; Vogt, A.; Müller, M.; Koch, H.-G. Protein translocation across the inner membrane of Gram-negative bacteria: The Sec and Tat dependent protein transport pathways. Res. Microbiol. 2013, 164, 505–534. [Google Scholar] [CrossRef] [PubMed]
- Angelini, S.; Deitermann, S.; Koch, H.G. FtsY, the bacterial signal-recognition particle receptor, interacts functionally and physically with the SecYEG translocon. EMBO Reports 2005, 6, 476–481. [Google Scholar] [CrossRef] [Green Version]
- Tsirigotaki, A.; De Geyter, J.; Šoštaric, N.; Economou, A.; Karamanou, S. Protein export through the bacterial Sec pathway. Nat. Rev. Micro. 2017, 15, 21. [Google Scholar] [CrossRef]
- Palmer, T.; Berks, B.C. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Micro. 2012, 10, 483–496. [Google Scholar] [CrossRef]
- Berks, B.C. The twin-arginine protein translocation pathway. Annu. Rev. Biochem. 2015, 84, 843–864. [Google Scholar] [CrossRef] [Green Version]
- Zhang, J.z.; Popov, V.L.; Gao, S.; Walker, D.H.; Yu, X.j. The developmental cycle of Ehrlichia chaffeensis in vertebrate cells. Cell. Microbiol. 2007, 9, 610–618. [Google Scholar] [CrossRef] [PubMed]
- Rikihisa, Y. Anaplasma phagocytophilum and Ehrlichia chaffeensis: Subversive manipulators of host cells. Nat. Rev. Micro. 2010, 8, 328–339. [Google Scholar] [CrossRef]
- McLeod, M.P.; Qin, X.; Karpathy, S.E.; Gioia, J.; Highlander, S.K.; Fox, G.E.; McNeill, T.Z.; Jiang, H.; Muzny, D.; Jacob, L.S. Complete genome sequence of Rickettsia typhi and comparison with sequences of other rickettsiae. J. Bacteriol. 2004, 186, 5842–5855. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nakayama, K.; Yamashita, A.; Kurokawa, K.; Morimoto, T.; Ogawa, M.; Fukuhara, M.; Urakami, H.; Ohnishi, M.; Uchiyama, I.; Ogura, Y. The whole-genome sequencing of the obligate intracellular bacterium Orientia tsutsugamushi revealed massive gene amplification during reductive genome evolution. DNA Res. 2008, 15, 185–199. [Google Scholar] [CrossRef]
- Christensen, S.; Serbus, L.R. Comparative analysis of Wolbachia genomes reveals streamlining and divergence of minimalist two-component systems. G3: Genes|Genomes|Genetics 2015, 5, 983–996. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lin, M.; Zhang, C.; Gibson, K.; Rikihisa, Y. Analysis of complete genome sequence of Neorickettsia risticii: Causative agent of Potomac horse fever. Nucleic Acids Res. 2009, 37, 6076–6091. [Google Scholar] [CrossRef] [PubMed]
- Klinges, J.G.; Rosales, S.M.; McMinds, R.; Shaver, E.C.; Shantz, A.A.; Peters, E.C.; Eitel, M.; Wörheide, G.; Sharp, K.H.; Burkepile, D.E. Phylogenetic, genomic, and biogeographic characterization of a novel and ubiquitous marine invertebrate-associated Rickettsiales parasite, Candidatus Aquarickettsia rohweri, gen. nov., sp. nov. The ISME journal 2019, 13, 2938–2953. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sassera, D.; Lo, N.; Epis, S.; D’Auria, G.; Montagna, M.; Comandatore, F.; Horner, D.; Peretó, J.; Luciano, A.M.; Franciosi, F. Phylogenomic evidence for the presence of a flagellum and cbb 3 oxidase in the free-living mitochondrial ancestor. Mol. Biol. Evol. 2011, 28, 3285–3296. [Google Scholar] [CrossRef]
- Rovery, C.; Renesto, P.; Crapoulet, N.; Matsumoto, K.; Parola, P.; Ogata, H.; Raoult, D. Transcriptional response of Rickettsia conorii exposed to temperature variation and stress starvation. Res. Microbiol. 2005, 156, 211–218. [Google Scholar] [CrossRef]
- Nelson, C.M.; Herron, M.J.; Felsheim, R.F.; Schloeder, B.R.; Grindle, S.M.; Chavez, A.O.; Kurtti, T.J.; Munderloh, U.G. Whole genome transcription profiling of Anaplasma phagocytophilum in human and tick host cells by tiling array analysis. BMC Genomics 2008, 9, 364. [Google Scholar] [CrossRef] [Green Version]
- Gillespie, J.J.; Brayton, K.A.; Williams, K.P.; Diaz, M.A.Q.; Brown, W.C.; Azad, A.F.; Sobral, B.W. Phylogenomics reveals a diverse Rickettsiales type IV secretion system. Infect. Immun. 2010, 78, 1809–1823. [Google Scholar] [CrossRef] [Green Version]
- Newton, I.L.; Slatko, B.E. Symbiosis comes of age at the 10th biennial meeting of Wolbachia researchers. Am Soc. Microbiol. 2019. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tatusova, T.; DiCuccio, M.; Badretdin, A.; Chetvernin, V.; Nawrocki, E.P.; Zaslavsky, L.; Lomsadze, A.; Pruitt, K.D.; Borodovsky, M.; Ostell, J. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016, 44, 6614–6624. [Google Scholar] [CrossRef] [PubMed]
- Haft, D.H.; DiCuccio, M.; Badretdin, A.; Brover, V.; Chetvernin, V.; O’Neill, K.; Li, W.; Chitsaz, F.; Derbyshire, M.K.; Gonzales, N.R. RefSeq: An update on prokaryotic genome annotation and curation. Nucleic Acids Res. 2018, 46, D851–D860. [Google Scholar] [CrossRef]
- Lindsey, A.R.I.; Rice, D.W.; Bordenstein, S.R.; Brooks, A.W.; Bordenstein, S.R.; Newton, I.L.G. Evolutionary genetics of cytoplasmic incompatibility genes cifA and cifB in prophage WO of Wolbachia. Genome Biol. Evol. 2018, 10, 434–451. [Google Scholar] [CrossRef]
- Bhattacharya, T.; Newton, I.L. Mi Casa es Su Casa: How an intracellular symbiont manipulates host biology. Environ. Microbiol. 2017, 21, 3188–3196. [Google Scholar] [CrossRef]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2014; Available online: URL http://www.R-project.org/ (accessed on 23 April 2010).
- Warnes, M.G.R.; Bolker, B.; Bonebakker, L.; Gentleman, R.; Huber, W. gplots: Various R Programming Tools for Plotting Data; ScienceOpen, Inc.: Middlesex Turnpike Burlington, MA, USA, 2016. [Google Scholar]
- Römling, U.; Gomelsky, M.; Galperin, M.Y. C-di-GMP: The dawning of a novel bacterial signalling system. Mol. Microbiol. 2005, 57, 629–639. [Google Scholar] [CrossRef] [PubMed]
- Tamayo, R.; Pratt, J.T.; Camilli, A. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu. Rev. Microbiol. 2007, 61, 131–148. [Google Scholar] [CrossRef] [Green Version]
- Del Medico, L.; Cerletti, D.; Schächle, P.; Christen, M.; Christen, B. The type IV pilin PilA couples surface attachment and cell–cycle initiation in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 2020, 117, 9546–9553. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brilli, M.; Fondi, M.; Fani, R.; Mengoni, A.; Ferri, L.; Bazzicalupo, M.; Biondi, E.G. The diversity and evolution of cell cycle regulation in alpha-proteobacteria: A comparative genomic analysis. BMC Systems Biology 2010, 4, 52. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Narayanan, S.; Kumar, L.; Radhakrishnan, S.K. Sensory domain of the cell cycle kinase CckA regulates the differential DNA binding of the master regulator CtrA in Caulobacter crescentus. Biochim. Biophys. Acta (BBA)-Gene Regul. Mech. 2018, 1861, 952–961. [Google Scholar] [CrossRef]
- Leung, M.M.; Brimacombe, C.A.; Beatty, J.T. Transcriptional regulation of the Rhodobacter capsulatus response regulator CtrA. Microbiology 2013, 159, 96. [Google Scholar] [CrossRef] [Green Version]
- Hallez, R.; Bellefontaine, A.-F.; Letesson, J.-J.; De Bolle, X. Morphological and functional asymmetry in α-proteobacteria. Trends Microbiol. 2004, 12, 361–365. [Google Scholar] [CrossRef]
- Cheng, Z.; Kumagai, Y.; Lin, M.; Zhang, C.; Rikihisa, Y. Intra-leukocyte expression of two-component systems in Ehrlichia chaffeensis and Anaplasma phagocytophilum and effects of the histidine kinase inhibitor closantel. Cell. Microbiol. 2006, 8, 1241–1252. [Google Scholar] [CrossRef] [PubMed]
- Lai, T.-H.; Kumagai, Y.; Hyodo, M.; Hayakawa, Y.; Rikihisa, Y. The Anaplasma phagocytophilum PleC histidine kinase and PleD diguanylate cyclase two-component system and role of cyclic Di-GMP in host cell infection. J. Bacteriol. 2009, 191, 693–700. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kumagai, Y.; Cheng, Z.; Lin, M.; Rikihisa, Y. Biochemical activities of three pairs of Ehrlichia chaffeensis two-component regulatory system proteins involved in inhibition of lysosomal fusion. Infect. Immun. 2006, 74, 5014–5022. [Google Scholar] [CrossRef] [Green Version]
- Paget, M.S. Bacterial sigma factors and anti-sigma factors: Structure, function and distribution. Biomolecules 2015, 5, 1245–1265. [Google Scholar] [CrossRef] [PubMed]
- Browning, D.F.; Busby, S.J. The regulation of bacterial transcription initiation. Nat. Rev. Micro. 2004, 2, 57–65. [Google Scholar] [CrossRef] [PubMed]
- Balleza, E.; Lopez-Bojorquez, L.N.; Martínez-Antonio, A.; Resendis-Antonio, O.; Lozada-Chávez, I.; Balderas-Martínez, Y.I.; Encarnación, S.; Collado-Vides, J. Regulation by transcription factors in bacteria: Beyond description. FEMS Microbiol. Rev. 2008, 33, 133–151. [Google Scholar] [CrossRef] [Green Version]
- Browning, D.F.; Butala, M.; Busby, S.J. Bacterial Transcription Factors: Regulation by Pick ‘N’Mix. J. Mol. Biol. 2019. [Google Scholar] [CrossRef]
- Martınez-Antonio, A.; Collado-Vides, J. Identifying global regulators in transcriptional regulatory networks in bacteria. Curr. Opin. Microbiol. 2003, 6, 482–489. [Google Scholar] [CrossRef] [PubMed]
- Meyer, R.R.; Laine, P.S. The single-stranded DNA-binding protein of Escherichia coli. Microbiol. Mol. Biol. Rev. 1990, 54, 342–380. [Google Scholar] [CrossRef]
- Dorman, C.J.; Deighan, P. Regulation of gene expression by histone-like proteins in bacteria. Curr. Opin. Genet. Dev. 2003, 13, 179–184. [Google Scholar] [CrossRef]
- Wei, L.; Wu, Y.; Qiao, H.; Xu, W.; Zhang, Y.; Liu, X.; Wang, Q. YebC controls virulence by activating T3SS gene expression in the pathogen Edwardsiella piscicida. FEMS Microbiol. Lett. 2018, 365, fny137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liang, H.; Li, L.; Dong, Z.; Surette, M.G.; Duan, K. The YebC family protein PA0964 negatively regulates the Pseudomonas aeruginosa quinolone signal system and pyocyanin production. J. Bacteriol. 2008, 190, 6217–6227. [Google Scholar] [CrossRef] [Green Version]
- Dressaire, C.; Moreira, R.N.; Barahona, S.; de Matos, A.P.A.; Arraiano, C.M. BolA is a transcriptional switch that turns off motility and turns on biofilm development. mBio 2015, 6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Santos, J.M.; Freire, P.; Vicente, M.; Arraiano, C.M. The stationary-phase morphogene bolA from Escherichia coli is induced by stress during early stages of growth. Mol. Microbiol. 1999, 32, 789–798. [Google Scholar] [CrossRef] [Green Version]
- Aldea, M.; Garrido, T.; Hernández-Chico, C.; Vicente, M.; Kushner, S. Induction of a growth-phase-dependent promoter triggers transcription of bolA, an Escherichia coli morphogene. EMBO J. 1989, 8, 3923–3931. [Google Scholar] [CrossRef]
- Freire, P.; Moreira, R.N.; Arraiano, C.M. BolA inhibits cell elongation and regulates MreB expression levels. J. Mol. Biol. 2009, 385, 1345–1351. [Google Scholar] [CrossRef]
- Brown, A.M.; Wasala, S.K.; Howe, D.K.; Peetz, A.B.; Zasada, I.A.; Denver, D.R. Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts. Sci. Rep. 2016, 6, 34955. [Google Scholar] [CrossRef]
- Gerth, M.; Bleidorn, C. Comparative genomics provides a timeframe for Wolbachia evolution and exposes a recent biotin synthesis operon transfer. Nat. Micro. 2016, 2, 16241. [Google Scholar] [CrossRef] [PubMed]
- Ward, C.M.; Baxter, S.W. Draft genome assembly of a Wolbachia endosymbiont of Plutella australiana. Genome Announc. 2017, 5. [Google Scholar] [CrossRef] [Green Version]
- Borukhov, S.; Lee, J.; Laptenko, O. Bacterial transcription elongation factors: New insights into molecular mechanism of action. Mol. Microbiol. 2005, 55, 1315–1324. [Google Scholar] [CrossRef]
- Borukhov, S.; Polyakov, A.; Nikiforov, V.; Goldfarb, A. GreA protein: A transcription elongation factor from Escherichia coli. Proc. Natl. Acad. Sci. USA 1992, 89, 8899–8902. [Google Scholar] [CrossRef] [Green Version]
- Kusuya, Y.; Kurokawa, K.; Ishikawa, S.; Ogasawara, N.; Oshima, T. Transcription factor GreA contributes to resolving promoter-proximal pausing of RNA polymerase in Bacillus subtilis cells. J. Bacteriol. 2011, 193, 3090–3099. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nag, J.K.; Shrivastava, N.; Chahar, D.; Gupta, C.L.; Bajpai, P.; Misra-Bhattacharya, S. Wolbachia Transcription Elongation Factor “Wol GreA” Interacts with α2ββ′ σ Subunits of RNA Polymerase through Its Dimeric C-Terminal Domain. PLoS Negl. Trop. Dis. 2014, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Slatko, B.E.; Taylor, M.J.; Foster, J.M. The Wolbachia endosymbiont as an anti-filarial nematode target. Symbiosis 2010, 51, 55–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brennan, C.A.; Dombroski, A.J.; Platt, T. Transcription termination factor rho is an RNA-DNA helicase. Cell 1987, 48, 945–952. [Google Scholar] [CrossRef]
- Farnham, P.J.; Platt, T. Rho-independent termination: Dyad symmetry in DNA causes RNA polymerase to pause during transcription in vitro. Nucleic Acids Res. 1981, 9, 563–577. [Google Scholar] [CrossRef]
- Lesnik, E.A.; Sampath, R.; Levene, H.B.; Henderson, T.J.; McNeil, J.A.; Ecker, D.J. Prediction of rho-independent transcriptional terminators in Escherichia coli. Nucleic Acids Res. 2001, 29, 3583–3594. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nudler, E.; Mironov, A.S. The riboswitch control of bacterial metabolism. Trends Biochem. Sci. 2004, 29, 11–17. [Google Scholar] [CrossRef] [PubMed]
- Nudler, E.; Gottesman, M.E. Transcription termination and anti-termination in E. coli. Genes Cells 2002, 7, 755–768. [Google Scholar] [CrossRef] [PubMed]
- Beckmann, J.F.; Bonneau, M.; Chen, H.; Hochstrasser, M.; Poinsot, D.; Merçot, H.; Weill, M.; Sicard, M.; Charlat, S. The toxin-antidote model of cytoplasmic incompatibility: Genetics and evolutionary implications. Trends Genet. 2019. [Google Scholar] [CrossRef]
- Peabody, C.R.; Chung, Y.J.; Yen, M.-R.; Vidal-Ingigliardi, D.; Pugsley, A.P.; Saier Jr, M.H. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 2003, 149, 3051–3072. [Google Scholar] [CrossRef] [PubMed]
- Fuche, F.; Vianney, A.; Andrea, C.; Doublet, P.; Gilbert, C. Functional type 1 secretion system involved in Legionella pneumophila virulence. J. Bacteriol. 2015, 197, 563–571. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brown, C.L.; Garner, E.; Jospin, G.; Coil, D.A.; Schwake, D.O.; Eisen, J.A.; Mukhopadhyay, B.; Pruden, A.J. Whole genome sequence analysis reveals the broad distribution of the RtxA type 1 secretion system and four novel putative type 1 secretion systems throughout the Legionella genus. PLoS One 2020, 15, e0223033. [Google Scholar] [CrossRef] [Green Version]
- Kaur, S.J.; Rahman, M.S.; Ammerman, N.C.; Beier-Sexton, M.; Ceraul, S.M.; Gillespie, J.J.; Azad, A.F. TolC-dependent secretion of an ankyrin repeat-containing protein of Rickettsia typhi. J. Bacteriol. 2012, 194, 4920–4932. [Google Scholar] [CrossRef] [Green Version]
- VieBrock, L.; Evans, S.M.; Beyer, A.R.; Larson, C.L.; Beare, P.A.; Ge, H.; Singh, S.; Rodino, K.G.; Heinzen, R.A.; Richards, A.L. Orientia tsutsugamushi ankyrin repeat-containing protein family members are Type 1 secretion system substrates that traffic to the host cell endoplasmic reticulum. Frontiers in Cellular and Infection Microbiology 2015, 4, 186. [Google Scholar] [CrossRef]
- Wakeel, A.; den Dulk-Ras, A.; Hooykaas, P.J.; McBride, J.W. Ehrlichia chaffeensis tandem repeat proteins and Ank200 are type 1 secretion system substrates related to the repeats-in-toxin exoprotein family. Front. Cell. Infect. Microbiol. 2011, 1, 22. [Google Scholar] [CrossRef] [Green Version]
- Pichon, S.; Bouchon, D.; Cordaux, R.; Chen, L.; Garrett, R.A.; Grève, P. Conservation of the Type IV secretion system throughout Wolbachia evolution. Biochem. Biophys. Res. Commun. 2009, 385, 557–562. [Google Scholar] [CrossRef]
- Carpinone, E.M.; Li, Z.; Mills, M.K.; Foltz, C.; Brannon, E.R.; Carlow, C.K.; Starai, V.J. Identification of putative effectors of the Type IV secretion system from the Wolbachia endosymbiont of Brugia malayi. PLoS ONE 2018, 13. [Google Scholar] [CrossRef]
- Pichon, S.; Bouchon, D.; Liu, C.; Chen, L.; Garrett, R.; Greve, P. The expression of one ankyrin pk2 allele of the WO prophage is correlated with the Wolbachia feminizing effect in isopods. BMC Microbiol. 2012, 12, 55. [Google Scholar] [CrossRef] [Green Version]
- Whitaker, N.; Berry, T.M.; Rosenthal, N.; Gordon, J.E.; Gonzalez-Rivera, C.; Sheehan, K.B.; Truchan, H.K.; VieBrock, L.; Newton, I.L.; Carlyon, J.A. Chimeric coupling proteins mediate transfer of heterologous type IV effectors through the Escherichia coli pKM101-encoded conjugation machine. J. Bacteriol. 2016, 198, 2701–2718. [Google Scholar] [CrossRef] [Green Version]
- Ellegaard, K.M.; Klasson, L.; Naslund, K.; Bourtzis, K.; Andersson, S.G.E. Comparative genomics of Wolbachia and the bacterial species concept. PLoS Genet. 2013, 9, e1003381. [Google Scholar] [CrossRef] [Green Version]
- Jacob, F.; Monod, J. Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 1961, 3, 318–356. [Google Scholar] [CrossRef]
- Darby, A.C.; Gill, A.C.; Armstrong, S.D.; Hartley, C.S.; Xia, D.; Wastling, J.M.; Makepeace, B.L. Integrated transcriptomic and proteomic analysis of the global response of Wolbachia to doxycycline-induced stress. ISME J. 2014, 8, 925–937. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gutzwiller, F.; Carmo, C.R.; Miller, D.E.; Rice, D.W.; Newton, I.L.; Hawley, R.S.; Teixeira, L.; Bergman, C.M. Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle. G3: Genes Genomes Genet. 2015, 5, 2843–2856. [Google Scholar] [CrossRef] [Green Version]
- Bennuru, S.; Meng, Z.; Ribeiro, J.M.; Semnani, R.T.; Ghedin, E.; Chan, K.; Lucas, D.A.; Veenstra, T.D.; Nutman, T.B. Stage-specific proteomic expression patterns of the human filarial parasite Brugia malayi and its endosymbiont Wolbachia. Proc. Natl. Acad. Sci. USA 2011, 108, 9649–9654. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bennuru, S.; Cotton, J.A.; Ribeiro, J.M.; Grote, A.; Harsha, B.; Holroyd, N.; Mhashilkar, A.; Molina, D.M.; Randall, A.Z.; Shandling, A.D.; et al. Stage-specific transcriptome and proteome analyses of the filarial parasite Onchocerca volvulus and its Wolbachia endosymbiont. mBio 2016, 7. [Google Scholar] [CrossRef] [Green Version]
- Darby, A.C.; Armstrong, S.D.; Bah, G.S.; Kaur, G.; Hughes, M.A.; Kay, S.M.; Koldkjær, P.; Rainbow, L.; Radford, A.D.; Blaxter, M.L. Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res. 2012, 22, 2467–2477. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luck, A.N.; Evans, C.C.; Riggs, M.D.; Foster, J.M.; Moorhead, A.R.; Slatko, B.E.; Michalski, M.L. Concurrent transcriptional profiling of Dirofilaria immitis and its Wolbachia endosymbiont throughout the nematode life cycle reveals coordinated gene expression. BMC Genomics 2014, 15, 1041. [Google Scholar] [CrossRef] [Green Version]
- Shropshire, J.D.; Bordenstein, S.R. Two-By-One model of cytoplasmic incompatibility: Synthetic recapitulation by transgenic expression of cifA and cifB in Drosophila. PLoS Genet. 2019, 15. [Google Scholar] [CrossRef] [Green Version]
- Shropshire, J.D.; On, J.; Layton, E.M.; Zhou, H.; Bordenstein, S.R. One prophage WO gene rescues cytoplasmic incompatibility in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 2018, 115, 4987–4991. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pietri, J.E.; DeBruhl, H.; Sullivan, W. The rich somatic life of Wolbachia. Microbiol. Open 2016. [Google Scholar] [CrossRef] [PubMed]
- Vavre, F.; Fleury, F.; Lepetit, D.; Fouillet, P.; Bouletreau, M. Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol. Biol. Evol. 1999, 16, 1711–1723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bonhag, P.F. Ovarian structure and vitellogenesis in insects. Annu. Rev. Entomol. 1958, 3, 137–160. [Google Scholar] [CrossRef]
- Berger, B.R.; Christie, P.J. Genetic complementation analysis of the Agrobacterium tumefaciens virB operon: virB2 through virB11 are essential virulence genes. J. Bacteriol. 1994, 176, 3646–3660. [Google Scholar] [CrossRef] [Green Version]
- Karna, S.R.; Zogaj, X.; Barker, J.R.; Seshu, J.; Dove, S.L.; Klose, K.E. A bacterial two-hybrid system that utilizes Gateway cloning for rapid screening of protein-protein interactions. BioTechniques 2010, 49, 831–833. [Google Scholar] [CrossRef] [Green Version]
- Massie, J.P.; Reynolds, E.L.; Koestler, B.J.; Cong, J.-P.; Agostoni, M.; Waters, C.M. Quantification of high-specificity cyclic diguanylate signaling. Proc. Natl. Acad. Sci. USA 2012, 109, 12746–12751. [Google Scholar] [CrossRef] [Green Version]
- Lindsey, A.R.; Bhattacharya, T.; Hardy, R.W.; Newton, I. Wolbachia and virus alter the host transcriptome at the interface of nucleotide metabolism pathways. bioRxiv 2020. [Google Scholar]
- Jayaram, N.; Usvyat, D.; Martin, A.C. Evaluating tools for transcription factor binding site prediction. BMC Bioinform. 2016, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mundade, R.; Ozer, H.G.; Wei, H.; Prabhu, L.; Lu, T. Role of ChIP-seq in the discovery of transcription factor binding sites, differential gene regulation mechanism, epigenetic marks and beyond. Cell Cycle 2014, 13, 2847–2852. [Google Scholar] [CrossRef] [PubMed] [Green Version]
© 2020 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Lindsey, A.R.I. Sensing, Signaling, and Secretion: A Review and Analysis of Systems for Regulating Host Interaction in Wolbachia. Genes 2020, 11, 813. https://doi.org/10.3390/genes11070813
Lindsey ARI. Sensing, Signaling, and Secretion: A Review and Analysis of Systems for Regulating Host Interaction in Wolbachia. Genes. 2020; 11(7):813. https://doi.org/10.3390/genes11070813
Chicago/Turabian StyleLindsey, Amelia R. I. 2020. "Sensing, Signaling, and Secretion: A Review and Analysis of Systems for Regulating Host Interaction in Wolbachia" Genes 11, no. 7: 813. https://doi.org/10.3390/genes11070813
APA StyleLindsey, A. R. I. (2020). Sensing, Signaling, and Secretion: A Review and Analysis of Systems for Regulating Host Interaction in Wolbachia. Genes, 11(7), 813. https://doi.org/10.3390/genes11070813