Angomonas deanei

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Angomonas deanei
Angomonas deanei structure.TIF
Three-dimensional reconstruction of Angomonas deanei containing a bacterial endosymbiont (green) near its nucleus (blue).
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Phylum: Euglenozoa
Class: Kinetoplastea
Order: Trypanosomatida
Family: Trypanosomatidae
Genus: Angomonas
Species:
A. deanei
Binomial name
Angomonas deanei
(Carvalho, 1973)
Teixeira & Camargo, 2011 [1]
Synonyms

Crithidia deaneiCarvalho, 1973

Angomonas deanei is a flagellated trypanosomatid protozoan. As an obligate parasite, it infects the gastrointestinal tract of insects, and is in turn a host to symbiotic bacteria. The bacterial endosymbiont Ca. "Kinetoplastibacterium crithidii" maintains a permanent mutualistic relationship with the protozoan such that it is no longer able to reproduce and survive on its own. [2] The symbiosis, subsequently also discovered in varying degrees in other protists such as Strigomonas culicis, Novymonas esmeraldas, Diplonema japonicum and Diplonema aggregatum are considered as good models for the understanding of the evolution of eukaryotes from prokaryotes, [3] [4] [5] and on the origin of cell organelles (i.e. symbiogenesis). [6] [7]

Contents

The species was first described as Crithidia deanei in 1973 by a Brazilian parasitologist Aurora L. M. Carvalho. A phylogenetic analysis in 2011 revealed that it belongs to the genus Angomonas, thereby becoming Angomonas deanei. The symbiotic bacterium is a member of the β-proteobacterium that descended from the common ancestor with the genus Bordetella , [1] or more likely, Taylorella . [8] The two organisms have depended on each other so much that the bacterium cannot reproduce and the protozoan can no longer infect insects when they are isolated. [9] [10]

Discovery

Angomonas deanei was originally described as Crithidia deanei. In 1973, a Brazilian graduate student Aurora Luiza de Moura Carvalho at the Universidade Federal de Goiás [11] discovered the species from his study of intestinal parasites of the assassin bugs in Goiás. [12] The next year he reported that the bug Zelus leucogrammus from which he discovered was not naturally infected by the protozoan, but it was acquired from other insects. [11] At the same time, a research team at the Universidade de Brasilia reported the biochemical properties and structural details based on transmission electron microscopy. They discovered that it harbours an endosymbiont, describing it as "probably bacterial" that provided the "trypanosomatid essential nutrients." [13] The bacterial nature of the endosymbiont was confirmed in 1977 when it was shown that it could be killed by treating with an antibiotic chloramphenicol, [14] and that it helps the host in synthesising the amino acid arginine from ornithine. [15]

As more structural and molecular details were studied, the distinction of A. deanei from other Crithidia species became more pronounced. In 1991, Maria Auxiliadora de Sousa and Suzana Corte-Real at the Instituto Oswaldo Cruz proposed a new genus Angomonas for the species. [16] [17] Phylogenetic study by Marta M.G. Teixeira and Erney P. Camargo at the University of São Paulo with their collaborators in 2011 validated the new species name A. deanei along with a description of a new related species A. ambiguus, which also contains the same bacterial endosymbiont. [1]

Structure

Ultrastructure and morphology of Angomonas deanei. (a) Transmission electron microscopy of the main cell body showing nucleus (nu) with heterochromatins (ht), kinetoplast (k) and bacterial symbiont (s). (b) Magnified view of the kinetoplast region showing a group of kDNA fibres. (c) Scanning electron microscopy of the protozoans; the projection from each individual is a flagellum. Angomonas deanei.jpg
Ultrastructure and morphology of Angomonas deanei. (a) Transmission electron microscopy of the main cell body showing nucleus (nu) with heterochromatins (ht), kinetoplast (k) and bacterial symbiont (s). (b) Magnified view of the kinetoplast region showing a group of kDNA fibres. (c) Scanning electron microscopy of the protozoans; the projection from each individual is a flagellum.

The body of Angomonas deanei is elliptical in shape, with a prominent tail-like flagellum at its posterior end for locomotion. The bacterial endosymbiont is inside its body and is surrounded by two cell membranes typical of Gram-negative bacteria, but its cell membrane presents unusual features, such as the presence of phosphatidylcholine, a major membrane lipid (atypical of bacterial membranes), and the highly reduced peptidoglycan layer, which shows reduced or absence of rigid cell wall. The cell membrane of the protozoan host contains an 18-domain β-barrel porin, which is a characteristic protein of Gram-negative bacteria, and unusual of eukaryotes. [18] In addition it contains cardiolipin and phosphatidylcholine as the major phospholipids, while sterols are absent. [19] Cardiolipin is a typical lipid of bacterial membranes; phosphatidylcholine, on the other hand, is mostly present in symbiotic prokaryotes of eukaryotic cells. For symbiotic adaptation, the protozoan host has undergone alterations such as reduced paraflagellar rod, which is required for full motility of the bacterial flagella. Yet the paraflagellar rod gene PFR1 is fully functional. [20] It also lacks introns and transcription of long polycistronic mRNAs required by other eukaryotes for complex gene activities. [21] Its entire genome is distributed in 29 chromosomes and contains 10,365 protein-coding genes, 59 transfer RNAs, 26 ribosomal RNAs, and 62 noncoding RNAs. [22]

While the protozoan has its separate mitochondria that provide electron transport system for the production of cellular energy, the ATP molecules are produced through its glycosomes. [9] The bacterium is known to provide essential nutrients to the host. It synthesises amino acids, [23] vitamins, [24] nitrogenous bases and haem [25] for the protozoan. Haem is necessary for the growth and development of the protozoan. [21] The bacterium also provides the enzymes for urea cycle which are absent in the host. In return the protozoan offers its enzymes for the complete metabolic pathways for the biosynthesis of amino acids, lipids and nucleotides, that are absent in the bacterium. [26] The bacterium has highly reduced genome compared to its related bacterial species, lacking many genes essential for its survival. [21] Phosphatidylinositol, a membrane lipid required for cell-cell interaction in the bacteria is also synthesised by the protozoan. [27] The bacterium also depends on the host for ATP molecules for its energetic functions. Thus, the two organisms intimately share and exchange their metabolic systems. [9]

When the bacterium is killed using antibiotics, the protozoan can no longer infect insects, [10] due to the altered glycosylphosphatidylinositol (gp63) in the protozoan flagellum. [28] A bacterium-less protozoan exhibits reduced gene activities; particularly those involved in oxidation-reduction process, ATP hydrolysis-coupled proton transport and glycolysis are stopped. [29] The structural components are also altered including cell surface, carbohydrate composition, paraflagellar rod and kinetoplast. [30]

Parasitism

Angomonas deanei was originally discovered from the digestive tract of the bug Zelus leucogrammus . But it was realised that the bugs are not heavily infected and were likely transmitted from other insects. [11] It is now known to infect different mosquitos, [31] and flies, [32] and capable of infecting mammalian fibroblast cells under experimental conditions. [33] [34] Transmission from one insect to another occurs between adults (horizontal transmission) only, and the protozoan cannot fix itself in the hindgut of insect larvae. The flagellum is used as an adhesive organ that gets attached near the rectal glands and sometime directly on the surface of the rectal glands. [35]

Reproduction

Angomonas deanei (light-blue is its nucleus) coordinated division with its symbiotic bacterium (green)

The cellular reproduction shows a strong synergistic adaptation between the bacterium and the protozoan. The bacterium divides first, followed by the protozoan organelles, and lastly the nucleus. As a result the daughter protozoans contains exactly the same copies of the organelles and the bacterial endosymbiont. [36] The entire reproduction takes about 6 hours in an ideal culture medium; thus, a single protozoan is able to produce 256 daughter cells in a day, though it can differ slightly under its natural habitat. [21]

The endosymbiont and evolution

Symbiotic bacteria in the trypanosomatid protozoa are descended from a β-proteobacterium. [37] With A. deanei, the bacteria Ca. " Kinetoplastibacterium crithidii" have co-evolved in a mutualistic relationship characterised by intense metabolic exchanges. The endosymbiont contains enzymes and metabolic precursors that complete essential biosynthetic pathways of the host protozoan, such as those in the urea cycle and the production of haemin and polyamine. [38]

The symbiotic bacterium belongs to β-proteobacterium family Alcaligenaceae. Based on the 16S rRNA gene sequences, it is known that it originated from a common ancestor with the one in Strigomonas culicis . The two groups are assumed to enter two different host protozoans to evolve into different species. Hence the scientific name ( Candidatus ) Kinetoplastibacterium crithidii was given to the bacterium. [39] Although it was initially proposed that the bacterium evolved from a common ancestor with members of Bordetella , [1] however, detailed phylogenomic analysis revealed that it is more closely related to members of the genus Taylorella . [8] Re-analysis by GTDB finds the genus sister to Proftella , a symbiont of Diaphorina citri . [40]

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<span class="mw-page-title-main">Symbiogenesis</span> Evolutionary theory holding that eukaryotic organelles evolved through symbiosis with prokaryotes

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References

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  4. ↑ 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.
  5. ↑ Tashyreva, Daria; Prokopchuk, Galina; Votýpka, Jan; Yabuki, Akinori; Horák, Aleš; Lukeš, Julius (2018-05-02). Heitman, Joseph (ed.). "Life Cycle, Ultrastructure, and Phylogeny of New Diplonemids and Their Endosymbiotic Bacteria". mBio. 9 (2). João M. P. Alves, John McCutcheon. doi:10.1128/mBio.02447-17. ISSN   2161-2129. PMC   5845003 . PMID   29511084.
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  7. ↑ Husnik, Filip; Keeling, Patrick J (2019). "The fate of obligate endosymbionts: reduction, integration, or extinction". Current Opinion in Genetics & Development. 58–59: 1–8. doi:10.1016/j.gde.2019.07.014. PMID   31470232. S2CID   201731819.
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  12. ↑ Carvalho, Aurora Luiza de Moura (1973). "Estudos sobre a posição sistemática, a biologia e a transmissào de tripanosomatídeos encontrados em Zelus leucogrammus (Perty, 1834) (Hemiptera, Reduviidae)". Rev. Pat. Trop. (in Portuguese). 2 (2): 223–274.
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  14. ↑ Mundim, Maria Hermelinda; Roitman, Isaac (1977). "Extra Nutritional Requirements of Artificially Aposymbiotic Crithidia deanei *". The Journal of Protozoology. 24 (2): 329–331. doi:10.1111/j.1550-7408.1977.tb00988.x.
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  17. ↑ Teixeira, Marta M. G.; Takata, Carmen S. A.; Conchon, Ivete; Campaner, Marta; Camargo, Erney P. (1997). "Ribosomal and kDNA Markers Distinguish Two Subgroups of Herpetomonas among Old Species and New Trypanosomatids Isolated from Flies". The Journal of Parasitology. 83 (1): 58–65. doi:10.2307/3284317. JSTOR   3284317. PMID   9057697.
  18. ↑ Andrade Ida S, Vianez-Júnior JL, Goulart CL, Homblé F, Ruysschaert JM, Almeida von Krüger WM, Bisch PM, de Souza W, Mohana-Borges R, Motta MC (2011). "Characterization of a porin channel in the endosymbiont of the trypanosomatid protozoan Crithidia deanei". Microbiology. 157 (Pt 10): 2818–2830. doi: 10.1099/mic.0.049247-0 . PMID   21757490.
  19. ↑ Palmié-Peixoto IV, Rocha MR, Urbina JA, de Souza W, Einicker-Lamas M, Motta MC (2006). "Effects of sterol biosynthesis inhibitors on endosymbiont-bearing trypanosomatids". FEMS Microbiol Lett. 255 (1): 33–42. doi: 10.1111/j.1574-6968.2005.00056.x . PMID   16436059.
  20. ↑ Gadelha C, Wickstead B, de Souza W, Gull K, Cunha-e-Silva N (2005). "Cryptic paraflagellar rod in endosymbiont-containing kinetoplastid protozoa". Eukaryot Cell. 4 (3): 516–525. doi:10.1128/EC.4.3.516-525.2005. PMC   1087800 . PMID   15755914.
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  22. ↑ Davey, John W; Catta-Preta, Carolina M C; James, Sally; Forrester, Sarah; Motta, Maria Cristina M; Ashton, Peter D; Mottram, Jeremy C (2021). Andrews, B (ed.). "Chromosomal assembly of the nuclear genome of the endosymbiont-bearing trypanosomatid Angomonas deanei". G3: Genes, Genomes, Genetics. 11 (1): jkaa018. doi:10.1093/g3journal/jkaa018. ISSN   2160-1836. PMC   8022732 . PMID   33561222.
  23. ↑ Alves, João MP; Klein, Cecilia C; da Silva, Flávia; Costa-Martins, André G; Serrano, Myrna G; Buck, Gregory A; Vasconcelos, Ana Tereza R; Sagot, Marie-France; Teixeira, Marta MG; Motta, Maria Cristina M; Camargo, Erney P (2013). "Endosymbiosis in trypanosomatids: the genomic cooperation between bacterium and host in the synthesis of essential amino acids is heavily influenced by multiple horizontal gene transfers". BMC Evolutionary Biology. 13 (1): 190. doi: 10.1186/1471-2148-13-190 . PMC   3846528 . PMID   24015778.
  24. ↑ Klein, Cecilia C.; Alves, João M. P.; Serrano, Myrna G.; Buck, Gregory A.; Vasconcelos, Ana Tereza R.; Sagot, Marie-France; Teixeira, Marta M. G.; Camargo, Erney P.; Motta, Maria Cristina M.; Parkinson, John (2013). "Biosynthesis of vitamins and cofactors in bacterium-harbouring trypanosomatids depends on the symbiotic association as revealed by genomic analyses". PLOS ONE. 8 (11): e79786. Bibcode:2013PLoSO...879786K. doi: 10.1371/journal.pone.0079786 . PMC   3833962 . PMID   24260300.
  25. ↑ Alves, João M. P.; Voegtly, Logan; Matveyev, Andrey V.; Lara, Ana M.; da Silva, Flávia Maia; Serrano, Myrna G.; Buck, Gregory A.; Teixeira, Marta M. G.; Camargo, Erney P. (2011). "Identification and phylogenetic analysis of heme synthesis genes in trypanosomatids and their bacterial endosymbionts". PLOS ONE. 6 (8): e23518. Bibcode:2011PLoSO...623518A. doi: 10.1371/journal.pone.0023518 . PMC   3154472 . PMID   21853145.
  26. ↑ Motta MC, Martins AC, de Souza SS, Catta-Preta CM, Silva R, Klein CC, de Almeida LG, de Lima Cunha O, Ciapina LP, Brocchi M, Colabardini AC, de Araujo Lima B, Machado CR, de Almeida Soares CM, Probst CM, de Menezes CB, Thompson CE, Bartholomeu DC, Gradia DF, Pavoni DP, Grisard EC, Fantinatti-Garboggini F, Marchini FK, Rodrigues-Luiz GF, Wagner G, Goldman GH, Fietto JL, Elias MC, Goldman MH, Sagot MF, Pereira M, Stoco PH, de Mendonça-Neto RP, Teixeira SM, Maciel TE, de Oliveira Mendes TA, Ürményi TP, de Souza W, Schenkman S, de Vasconcelos AT (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.
  27. ↑ de Azevedo-Martins, Allan C; Alves, João MP; Garcia de Mello, Fernando; Vasconcelos, Ana Tereza R; de Souza, Wanderley; Einicker-Lamas, Marcelo; Motta, Maria Cristina M (2015). "Biochemical and phylogenetic analyses of phosphatidylinositol production in Angomonas deanei, an endosymbiont-harboring trypanosomatid". Parasites & Vectors. 8 (1): 247. doi: 10.1186/s13071-015-0854-x . PMC   4424895 . PMID   25903782.
  28. ↑ d'Avila-Levy CM, Santos LO, Marinho FA, Matteoli FP, Lopes AH, Motta MC, Santos AL, Branquinha MH (2008). "Crithidia deanei: influence of parasite gp63 homologue on the interaction of endosymbiont-harboring and aposymbiotic strains with Aedes aegypti midgut". Exp Parasitol. 118 (3): 345–353. doi:10.1016/j.exppara.2007.09.007. PMID   17945218.
  29. ↑ Penha, Luciana Loureiro; Hoffmann, Luísa; Souza, Silvanna Sant'Anna de; Martins, Allan Cézar de Azevedo; Bottaro, Thayane; Prosdocimi, Francisco; Faffe, Débora Souza; Motta, Maria Cristina Machado; Ürményi, Turán Péter; Silva, Rosane (2016). "Symbiont modulates expression of specific gene categories in Angomonas deanei". Memórias do Instituto Oswaldo Cruz. 111 (11): 686–691. doi:10.1590/0074-02760160228. PMC   5125052 . PMID   27706380.
  30. ↑ Souza, Wanderley; Motta, Maria Cristina Machado (1999). "Endosymbiosis in protozoa of the Trypanosomatidae family". FEMS Microbiology Letters. 173 (1): 1–8. doi: 10.1111/j.1574-6968.1999.tb13477.x . ISSN   0378-1097. PMID   10220875.
  31. ↑ D'Avila-Levy, Claudia M.; Silva, Bianca A.; Hayashi, Elize A.; Vermelho, Alane B.; Alviano, Celuta S.; Saraiva, Elvira M.B.; Branquinha, Marta H.; Santos, André L.S. (2005). "Influence of the endosymbiont of Blastocrithidia culicis and Crithidia deanei on the glycoconjugate expression and on Aedes aegypti interaction". FEMS Microbiology Letters. 252 (2): 279–286. doi: 10.1016/j.femsle.2005.09.012 . PMID   16216441.
  32. ↑ Borghesan, Tarcilla C.; Campaner, Marta; Matsumoto, Tania E.; Espinosa, Omar A.; Razafindranaivo, Victor; Paiva, Fernando; Carranza, Julio C.; Añez, Nestor; Neves, Luis; Teixeira, Marta M. G.; Camargo, Erney P. (2018). "Genetic Diversity and Phylogenetic Relationships of Coevolving Symbiont-Harboring Insect Trypanosomatids, and Their Neotropical Dispersal by Invader African Blowflies (Calliphoridae)". Frontiers in Microbiology. 9: 131. doi: 10.3389/fmicb.2018.00131 . PMC   5808337 . PMID   29467742.
  33. ↑ Santos, Dilvani O.; Bourguignon, Saulo C.; Castro, Helena Carla; Silva, Jonatan S.; Franco, Leonardo S.; Hespanhol, Renata; Soares, Maurilio J.; Corte-Real, Suzana (2004). "Infection of Mouse Dermal Fibroblasts by the Monoxenous Trypanosomatid Protozoa Crithidia deanei and Herpetomonas roitmani". The Journal of Eukaryotic Microbiology. 51 (5): 570–574. doi:10.1111/j.1550-7408.2004.tb00293.x. PMID   15537092. S2CID   5830694.
  34. ↑ Matteoli, Filipe P.; d’Avila-Levy, Claudia M.; Santos, Lívia O.; Barbosa, Gleyce M.; Holandino, Carla; Branquinha, Marta H.; Santos, André L.S. (2009). "Roles of the endosymbiont and leishmanolysin-like molecules expressed by Crithidia deanei in the interaction with mammalian fibroblasts". Experimental Parasitology. 121 (3): 246–253. doi:10.1016/j.exppara.2008.11.011. PMID   19070618.
  35. ↑ Ganyukova, Anna I.; Malysheva, Marina N.; Frolov, Alexander O. (2020). "Life cycle, ultrastructure and host-parasite relationships of Angomonas deanei (Kinetoplastea: Trypanosomatidae) in the blowfly Lucilia sericata (Diptera: Calliphoridae)" (PDF). Protistology. 14 (4): 204–218. doi: 10.21685/1680-0826-2020-14-4-2 .
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  37. ↑ Du Y, McLaughlin G, Chang KP (1994). "16S ribosomal DNA sequence identities of beta-proteobacterial endosymbionts in three Crithidia species". Journal of Bacteriology. 176 (10): 3081–3084. doi:10.1128/jb.176.10.3081-3084.1994. PMC   205468 . PMID   8188611.
  38. ↑ Frossard ML, Seabra SH, DaMatta RA, de Souza W, de Mello FG, Machado Motta MC (2006). "An endosymbiont positively modulates ornithine decarboxylase in host trypanosomatids". Biochem Biophys Res Commun. 343 (2): 443–449. doi:10.1016/j.bbrc.2006.02.168. PMID   16546131.
  39. ↑ Du Y, Maslov DA, Chang KP (1994). "Monophyletic origin of beta-division proteobacterial endosymbionts and their coevolution with insect trypanosomatid protozoa Blastocrithidia culicis and Crithidia spp". Proc Natl Acad Sci U S A. 91 (18): 8437–8441. Bibcode:1994PNAS...91.8437D. doi: 10.1073/pnas.91.18.8437 . PMC   44621 . PMID   7521530.
  40. ↑ "GTDB - Tree at g__Kinetoplastibacterium". gtdb.ecogenomic.org.
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