Strigomonas culicis

Strigomonas culicis is a protist and member of flagellated trypanosomatids. It is an obligate parasite in the gastrointestinal tract of mosquito, and is in turn a host to symbiotic bacteria. It maintains strict mutualistic relationship with the bacteria as a sort of cell organelle (endosymbiont) so that it cannot lead an independent life without the bacteria.[4][5] This and other symbiont-harbouring trypanosomatids such as Angomonas deanei are considered as "excellent models for the study of cell evolution because the host protozoan co-evolves with an intracellular bacterium in a mutualistic relationship",[6] and "the origin of new organelles" (i.e. symbiogenesis).[7]

Strigomonas culicis
Strigomonas culicis observed by differential interference contrast (DIC)[1]
Scientific classification
Domain:
Eukaryota
(unranked):
Excavata
Phylum:
Euglenozoa
Class:
Kinetoplastea
Order:
Trypanosomatida
Genus:
Strigomonas
Species:
culicis
Binomial name
Strigomonas culicis
Teixeira et al., 2011[2]
Synonyms

Blastocrithidia culicis Wallace and Johnson, 1961[3]

Originally described as Blastocrithidia culicis in 1961, it was renamed Strigomonas culicis in 2011 upon establishing its genetic relationship with other related protists.[2] The obligate bacterium belongs a group of ß-proteobacterium and provides nutrients to the host, in addition to influencing some of the cellular functions.[8]

Taxonomy

S. culicis was originally described as Blastocrithidia culicis by F.G. Wallace and A. Johnson in 1961.[3] It was later considered to be the same (synonym) as Trypanosoma (Herpetomonas) culicis, a species described by Frederick G. Novy,  Ward J. MacNeal, and Harry N. Torreyin 1907.[9] The species name refers to the mosquito Culex in which it was found. But it is also present in other mosquitos such as Aedes.[10] When Marta M.G. Teixeira and co-workers analysed the species in 2011 along with related protists such as Angomonas deanei using molecular techniques, it was resolved that it belonged to an already existing genus Strigomonas.[2]

Biology
Stages of dividing Strigomonas culicis with its bacterial symbiont - S (blue in 2 picture) and green indicate the bacterium; K denotes the kinetoplast, and N, the nucleus

S. culicis spends it life cycle in mosquitos. It migrates from the mosquito midgut and enter the body cavity (haemocoel) and finally reside in the salivary glands.[11] Unlike other trypanosomatids, S. culicis does not produce some amino acids such as methionine, histidine, and arginine; and vitamins such as thiamin, nicotinamide, and riboflavin.[10] The bacterium provides these nutrients. In addition, it also provides enzymes required by the host for amino acid synthesis, lipid and purine/pyrimidine metabolism, urea cycle, haeme biosynthesis,[6] protein synthesis, and protein folding. It can not reproduce on its own and relies on signals from the protist's nucleus.[5] Isolated bacteria cannot survive on their own.[6] When the bacteria are removed by antibiotic treatment, the protist survives but can not infect mosquitos.[5]

S. culicis has about 12,162 open reading frames (ORFs).[6]

The bacterium is member of ß-proteobacterium of the family Alcaligenaceae. It is enclosed in two layers of cell membranes, and unlike typical bacterial membrane, peptidoglycan is greatly reduced.[6] It acts as a cell organelle not only by supplying essential enzymes, but also by replacing paraflagellar rod associated to the axoneme, thus, intimately associated with the kinetoplast.[7] In addition, it provides surplus supply of ATP molecules for increased metabolic activities.[12] During cell division, as the kinetoplast of the host divides so do the bacterium.[13] The host cell controls the number of bacterial division.[1] This coordinated mitosis results in even distribution of one bacterium in each daughter cell.[13]

References
  1. Catta-Preta, Carolina M. C.; Brum, Felipe L.; da Silva, Camila C.; Zuma, Aline A.; Elias, Maria C.; de Souza, Wanderley; Schenkman, Sergio; Motta, Maria Cristina M. (2015). "Endosymbiosis in trypanosomatid protozoa: the bacterium division is controlled during the host cell cycle". Frontiers in Microbiology. 6: 520. doi:10.3389/fmicb.2015.00520. PMC 4451579. PMID 26082757.
  2. Teixeira, Marta M.G.; Borghesan, Tarcilla C.; Ferreira, Robson C.; Santos, Marcia A.; Takata, Carmen S.A.; Campaner, Marta; Nunes, Vania L.B.; Milder, Regina V.; de Souza, Wanderley; Camargo, Erney P. (2011). "Phylogenetic Validation of the Genera Angomonas and Strigomonas of Trypanosomatids Harboring Bacterial Endosymbionts with the Description of New Species of Trypanosomatids and of Proteobacterial Symbionts". Protist. 162 (3): 503–524. doi:10.1016/j.protis.2011.01.001. PMID 21420905.
  3. Wallace, F.G.; Johnson, A. (1961). "The infectivity of old cultured strains of mosquito flagellates". Journal of Insect Pathology. 3: 75–80.
  4. Chang, K. P. (1974). "Ultrastructure of symbiotic bacteria in normal and antibiotic-treated Blastocrithidia culicis and Crithidia oncopelti". The Journal of Protozoology. 21 (5): 699–707. doi:10.1111/j.1550-7408.1974.tb03733.x. PMID 4217371.
  5. Brunoro, Giselle V.F.; Menna-Barreto, Rubem F.S.; Garcia-Gomes, Aline S.; Boucinha, Carolina; Lima, Diogo B.; Carvalho, Paulo C.; Teixeira-Ferreira, André; Trugilho, Monique R.O.; Perales, Jonas; Schwämmle, Veit; Catanho, Marcos (2019). "Quantitative Proteomic Map of the Trypanosomatid Strigomonas culicis: The Biological Contribution of its Endosymbiotic Bacterium". Protist. 170 (6): 125698. doi:10.1016/j.protis.2019.125698. PMID 31760169.
  6. Motta, Maria Cristina Machado; Martins, Allan Cezar de Azevedo; de Souza, Silvana Sant'Anna; Catta-Preta, Carolina Moura Costa; Silva, Rosane; Klein, Cecilia Coimbra; de Almeida, Luiz Gonzaga Paula; de Lima Cunha, Oberdan; Ciapina, Luciane Prioli; Brocchi, Marcelo; Colabardini, Ana Cristina (2013). "Predicting the proteins of Angomonas deanei, Strigomonas culicis and their respective endosymbionts reveals new aspects of the trypanosomatidae family". PLOS ONE. 8 (4): e60209. Bibcode:2013PLoSO...860209M. doi:10.1371/journal.pone.0060209. PMC 3616161. PMID 23560078.
  7. de Souza, W.; Motta, M. C. (1999). "Endosymbiosis in protozoa of the Trypanosomatidae family". FEMS Microbiology Letters. 173 (1): 1–8. doi:10.1111/j.1574-6968.1999.tb13477.x. PMID 10220875.
  8. de Souza, Silvana Sant´Anna; Catta-Preta, Carolina Moura; Alves, João Marcelo P.; Cavalcanti, Danielle P.; Teixeira, Marta M. G.; Camargo, Erney P.; De Souza, Wanderley; Silva, Rosane; Motta, Maria Cristina M. (2017). Yurchenko, Vyacheslav (ed.). "Expanded repertoire of kinetoplast associated proteins and unique mitochondrial DNA arrangement of symbiont-bearing trypanosomatids". PLOS ONE. 12 (11): e0187516. Bibcode:2017PLoSO..1287516D. doi:10.1371/journal.pone.0187516. PMC 5683618. PMID 29131838.
  9. Novy, F. G.; MacNeal, W. J.; Torrey, H. N. (1907). "The Trypanosomes of Mosquitoes and Other Insects". Journal of Infectious Diseases. 4 (2): 223–276. doi:10.1093/infdis/4.2.223. JSTOR 30072673.
  10. de Menezez, Maria Claudia Noronha Dutra; Roitmanz, Isaac (1991). "Nutritional Requirements of Blastocrithidia culicis , a Trypanosomatid with an Endosymbiont 1". The Journal of Protozoology. 38 (2): 122–123. doi:10.1111/j.1550-7408.1991.tb06030.x.
  11. Catta-Preta, C.M.C.; Nascimento, M.T.C.; Garcia, M.C.F.; Saraiva, E.M.; Motta, M.C.M.; Meyer-Fernandes, J.R. (2013). "The presence of a symbiotic bacterium in Strigomonas culicis is related to differential ecto-phosphatase activity and influences the mosquito–protozoa interaction". International Journal for Parasitology. 43 (7): 571–577. doi:10.1016/j.ijpara.2013.02.005. PMID 23562935.
  12. Loyola-Machado, Ana Carolina; Azevedo-Martins, Allan Cézar; Catta-Preta, Carolina Moura Costa; de Souza, Wanderley; Galina, Antonio; Motta, Maria Cristina M. (2017). "The Symbiotic Bacterium Fuels the Energy Metabolism of the Host Trypanosomatid Strigomonas culicis". Protist. 168 (2): 253–269. doi:10.1016/j.protis.2017.02.001. PMID 28371652.
  13. Brum, Felipe Lopes; Catta-Preta, Carolina Moura Costa; de Souza, Wanderley; Schenkman, Sergio; Elias, Maria Carolina; Motta, Maria Cristina Machado (2014). "Structural characterization of the cell division cycle in Strigomonas culicis, an endosymbiont-bearing trypanosomatid". Microscopy and Microanalysis. 20 (1): 228–237. Bibcode:2014MiMic..20..228B. doi:10.1017/S1431927613013925. PMID 24397934.
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