Accessibility / Report Error

Ultrastructure of intracytoplasmic Rickettsia-like infection of the gills of the teleost Archosargus probatocephalus (Sparidae) in northeastern Brazil

Ultraestrutura de Rickettsia intracitoplasmática infectando as brânquias do teleósteo Archosargus probatocephalus (Sparidae) no Nordeste do Brasil

Abstract

A histopathological survey was conducted to investigate the presence of microparasites in fish Archosargus probatocephalus in a river near Maceió, Brazil. Light microscope observations of fragments of gill showed the presence of small cysts containing numerous myxospores that were morphologically identified as Henneguya. Transmission electron microscopy observations further revealed several gill cells containing groups of prokaryotic cells within large cytoplasmic vacuoles. Each infected host cell displayed a single vacuole containing a variable number of Rickettsia-like cells (up to 11), some of which presented the dumbbell shape characteristic of binary fission. The Rickettsia-like cells were pleomorphic, without a nucleus and with chromatin dispersed in the cytoplasm. They had a thin electron-dense wall of Gram-negative type. The morphology of these prokaryotic was similar to those of the order Rickettsiales and was described as a Rickettsia-like organism. Histopathological evaluation showed that several vacuole membranes had a lysed appearance. Some had ruptured, thus allowing direct contact between the Rickettsia-like organism and the cytoplasm of the host cell. The rupturing of the branchial epithelium may have contributed towards reduction of the surface area of the gills, but it is not possible to say that this was the cause of the host’s death.

Keywords:
Fish; Sparidae; cytoplasmic vacuoles; Rickettsia-like cell

Resumo

Um levantamento histopatológico foi realizado para pesquisar a presença de microparasitas, no peixe Archosargus probatocephalus, em um rio próximo a Maceió, Brasil. Observações ao microscópio óptico de fragmentos de brânquias mostraram a presença de pequenos cistos contendo numerosos mixósporos, identificados morfologicamente como Henneguya. Ocasionalmente, na microscopia eletrônica de transmissão, foram observados vários corpos citoplasmáticos de inclusão, grupo aparentemente de células procarióticas que vivem dentro de um grande vacúolo citoplasmático de algumas células branquiais. As células hospedeiras infectadas tinham um único vacúolo contendo um número variável de células do tipo Rickettsia, até 11, algumas das quais em forma do haltere, característica da fissão binária. Essas células eram pleomórficas sem núcleo, tendo a cromatina dispersa no citoplasma e possuíam uma parede densa de elétrons finos do tipo Gram-negativo. A morfologia dessas células procarióticas foi semelhante àquelas da ordem Rickettsiales e foram descritas como organismos tipo Rickettsiae. A histopatologia mostra várias membranas de vacúolos circundantes com aspetos lisados, enquanto outras apresentam rupturas que mostram contato direto do organismos tipo Rickettsiae com o citoplasma da célula hospedeira. A ruptura do epitélio branquial pode ter contribuído para a redução da superfície das brânquias, mas não é possível afirmar que foi a causa da morte do hospedeiro.

Palavras-chave:
Peixe; Sparidae; vacúolo citoplasmático; célula tipo Rickettsia

Introduction

Occurrences of cell-dependent prokaryotic microorganisms such as Bacteria, Rickettsiae, Mycoplasma and Chlamydia in eukaryotes has been described worldwide. These are commonly associated with differing pathogenicity in many geographical regions (Athanassopoulou & Karagouni, 2004Athanassopoulou F, Karagouni E. Rickettsia-like organisms (R.L.O.) infections of fin-fish. J Hell Vet Med Soc 2004; 55(2): 165-173. http://dx.doi.org/10.12681/jhvms.15188.
http://dx.doi.org/10.12681/jhvms.15188...
; Azevedo, 1993Azevedo C. Occurrence of an unusual branchial mycoplasma-like infection in cockle Cerastoderma edule (Mollusca, Bivalvia). Dis Aquat Organ 1993; 16: 55-59. http://dx.doi.org/10.3354/dao016055.
http://dx.doi.org/10.3354/dao016055...
; Azevedo et al., 2005Azevedo C, Padovan I, Corral L, Padovan P. Ultrastructural description of an unidentified apicomplexan oocyst containing bacteria-like hyperparasites in the gill of Crassostrea rizophorae. Dis Aquat Organ 2005; 65(2): 153-157. http://dx.doi.org/10.3354/dao065153. PMid:16060268.
http://dx.doi.org/10.3354/dao065153...
; Birkbecka & Ringøb, 2005Birkbecka TH, Ringøb E. Pathogenesis and the gastrointestinal tract of growing fish. Biol Grow Anim 2005; 2: 208-234. http://dx.doi.org/10.1016/S1877-1823(09)70043-8.
http://dx.doi.org/10.1016/S1877-1823(09)...
; Bower et al., 1994Bower SM, McGladdery SE, Price IM. Synopsis of infection diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 1994; 4: 1-199. http://dx.doi.org/10.1016/0959-8030(94)90028-0.
http://dx.doi.org/10.1016/0959-8030(94)9...
; Cusack et al., 2002Cusack RR, Groman DB, Jones SRM. Rickettsial infection in farmed Atlantic salmon in eastern Canada. Can Vet J 2002; 43(6): 435-440. PMid:12058568.; Fryer et al., 1990Fryer JL, Lannan CN, Garcés LH, Larenas JJ, Smith PA. Isolation of a rickettsiales-like organism from diseased coho salmon (Oncorhynchus kisutch) in Chile. Fish Pathol 1990; 25(2): 107-114. http://dx.doi.org/10.3147/jsfp.25.107.
http://dx.doi.org/10.3147/jsfp.25.107...
; Fryer & Lannan, 1994Fryer JL, Lannan CN. Rickettsial and chlamydial infections of freshwater and marine fishes, bivalves, and crustaceans. Zool Stud 1994; 33(2): 95-107.; Guo et al., 2004Guo Q, Jia W, Han X, Cai T, Gong X, Sun X. Rickettsia-like organism infection in a freshwater cultured fish Ophiocephalus argus C. in China. J Progr Nat Sci 2004; 14(5): 417-422. http://dx.doi.org/10.1080/10020070412331343711.
http://dx.doi.org/10.1080/10020070412331...
; Molloy et al., 2001Molloy DP, Giamberini L, Morado JF, Fokin SI, Laruelle F. Characterization of intracytoplasmic prokaryote infections in Dreissena sp. (Bivalvia: dreissenidae). Dis Aquat Organ 2001; 44(3): 203-216. http://dx.doi.org/10.3354/dao044203. PMid:11383568.
http://dx.doi.org/10.3354/dao044203...
; Turnbull, 1993Turnbull JF. Rickettsias and Chlamydias. In: Inglish V, Roberts RJ, Bromage NR. Bacterial Diseases of Fish. Oxford: Willey-Blackwell; 1993. p. 235-254.; Villalba et al., 1999Villalba A, Carballal MJ, López C, Cabada A, Corral L, Azevedo C. Branchial rickettsia-like infection associated with clam Venerupis rhomboides mortality. Dis Aquat Organ 1999; 36(1): 53-60. http://dx.doi.org/10.3354/dao036053.
http://dx.doi.org/10.3354/dao036053...
; Yuksel et al., 2006Yuksel SA, Thompson KD, Adams OA. Rickettsial infections of fish. Turk J Fish Aquat Sci 2006; 6: 63-78.). Rickettsial and bacterial diseases that affect a wide range of freshwater, brackish water and marine fish (Bower et al., 1994Bower SM, McGladdery SE, Price IM. Synopsis of infection diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 1994; 4: 1-199. http://dx.doi.org/10.1016/0959-8030(94)90028-0.
http://dx.doi.org/10.1016/0959-8030(94)9...
; Mauel et al., 2003Mauel MJ, Miller DL, Frazier K, Liggett AD, Styer L, Montgomery-Brock D, et al. Characterization of Piscirickettsiosis-like disease in Hawaiian tilapia. Dis Aquat Organ 2003; 53(3): 249-255. http://dx.doi.org/10.3354/dao053249. PMid:12691196.
http://dx.doi.org/10.3354/dao053249...
; Soares et al., 2013Soares S, Murray AG, Crumlish M, Turnbull JF, Green DM. Factors affecting variation in mortality of marine Atlantic salmon Salmo salar in Scotland. Dis Aquat Organ 2013; 103(2): 101-109. http://dx.doi.org/10.3354/dao02562. PMid:23548360.
http://dx.doi.org/10.3354/dao02562...
; Weinert et al., 2009Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM. Evolution and diversity of Rickettsia bacteria. BMC Biol 2009; 7(1): 6. http://dx.doi.org/10.1186/1741-7007-7-6. PMid:19187530.
http://dx.doi.org/10.1186/1741-7007-7-6...
), including ornamental species (Mauel et al., 2007Mauel MJ, Soto E, Moralis J, Hawke J. A piscirickettsiosis-like syndrome in cultured Nile tilapia in Latin America with a Francisella spp. as the pathogenic agent. J Aquat Anim Health 2007; 19(1): 27-34. http://dx.doi.org/10.1577/H06-025.1. PMid:18236629.
http://dx.doi.org/10.1577/H06-025.1...
) have been described. Elevated economic losses due to occurrences of rickettsial infections in cultivated fish have also frequently been reported (Branson & Diaz-Munoz, 1991Branson EJ, Diaz-Munoz DN. Description of a new disease condition occurring in farmed coho salmon, Oncorhynchus ksiutch (Walbaum), in South America. J Fish Dis 1991; 14(2): 147-156. http://dx.doi.org/10.1111/j.1365-2761.1991.tb00585.x.
http://dx.doi.org/10.1111/j.1365-2761.19...
; Chern & Chao, 1994Chern RS, Chao CB. Outbreaks of a disease caused by rickettsia-like organism in cultured tilapias in Taiwan. Fish Pathol 1994; 29(2): 61-71. http://dx.doi.org/10.3147/jsfp.29.61.
http://dx.doi.org/10.3147/jsfp.29.61...
; Corbeil et al., 2005Corbeil S, Hyatt AD, Crane MSJ. Characterisation of an emerging rickettsia-like organism in Tasmania farmed Atlantic salmon Salmo salar. Dis Aquat Organ 2005; 64(1): 37-44. http://dx.doi.org/10.3354/dao064037. PMid:15900686.
http://dx.doi.org/10.3354/dao064037...
; Cusack et al., 2002Cusack RR, Groman DB, Jones SRM. Rickettsial infection in farmed Atlantic salmon in eastern Canada. Can Vet J 2002; 43(6): 435-440. PMid:12058568.; Fryer et al., 1990Fryer JL, Lannan CN, Garcés LH, Larenas JJ, Smith PA. Isolation of a rickettsiales-like organism from diseased coho salmon (Oncorhynchus kisutch) in Chile. Fish Pathol 1990; 25(2): 107-114. http://dx.doi.org/10.3147/jsfp.25.107.
http://dx.doi.org/10.3147/jsfp.25.107...
; Mauel et al., 2003Mauel MJ, Miller DL, Frazier K, Liggett AD, Styer L, Montgomery-Brock D, et al. Characterization of Piscirickettsiosis-like disease in Hawaiian tilapia. Dis Aquat Organ 2003; 53(3): 249-255. http://dx.doi.org/10.3354/dao053249. PMid:12691196.
http://dx.doi.org/10.3354/dao053249...
).

Subsequently, several experiments have been conducted to evaluate the effects of different chemical biocide products on the development of rickettsial species (Mauel et al., 2003Mauel MJ, Miller DL, Frazier K, Liggett AD, Styer L, Montgomery-Brock D, et al. Characterization of Piscirickettsiosis-like disease in Hawaiian tilapia. Dis Aquat Organ 2003; 53(3): 249-255. http://dx.doi.org/10.3354/dao053249. PMid:12691196.
http://dx.doi.org/10.3354/dao053249...
; Miquel et al., 2003Miquel A, Müller I, Ferrer P, Valenzuela PDT, Burzio LO. Immunoresponse of Coho salmon immunized with a gene expression library from Piscirickettsia salmonis. Biol Res 2003; 36(3-4): 313-323. http://dx.doi.org/10.4067/S0716-97602003000300004. PMid:14631865.
http://dx.doi.org/10.4067/S0716-97602003...
; Palmer et al., 1996Palmer R, Ruttledge M, Callanan K, Drinan E. A Piscirickettsiosis-like disease in farmed Atlantic salmon in Ireland-isolation of the agent. Bull Eur Assoc Fish Pathol 1996; 17(2): 68-72.; Smith et al., 1996Smith PA, Vecchiola IM, Oyanedel S, Garcés LH, Larenas J, Contreras J. Antimicrobial sensitivity of four isolates of Piscirickettsia salmonis. Bull Eur Assoc Fish Pathol 1996; 16: 164-168.).

Over recent years, rickettsial diseases have been observed in various locations and in a variety of species, infecting different organs, how: the clam gills from Island Lizard (Great Barrier Reef) (Goggin & Lester, 1990Goggin GL, Lester RJG. Rickettsiales-like infection in the gill in Tridacna crocea from Great Barrier Reef. J Invertebr Pathol 1990; 56(1): 135-138. http://dx.doi.org/10.1016/0022-2011(90)90156-Z. PMid:2376662.
http://dx.doi.org/10.1016/0022-2011(90)9...
); the renal tissue of Chilean salmon (Oncorhynchus kisulch) (Fryer et al., 1992Fryer JL, Lannan CN, Giovannoni SJ, Wood ND. Piscirickettsia salmonis gen. nov., sp. nov., the causative agent of an epizootic disease in salmonid fishes. Int J Syst Bacteriol 1992; 42(1): 120-126. http://dx.doi.org/10.1099/00207713-42-1-120. PMid:1371057.
http://dx.doi.org/10.1099/00207713-42-1-...
); the gills of the oyster (Crassostrea gigas) collected in Spain and the digestive gland of the shrimp (Pandalus platyceros) from Canada (Bower et al., 1994Bower SM, McGladdery SE, Price IM. Synopsis of infection diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 1994; 4: 1-199. http://dx.doi.org/10.1016/0959-8030(94)90028-0.
http://dx.doi.org/10.1016/0959-8030(94)9...
) and the kidney, liver and spleen of juvenile Atractoscion nobilis, from the USA (Chen et al., 2000Chen MF, Yun S, Marty GD, McDowell TS, House ML, Appersen JA, et al. A Piscirickettsia salmonis-like bacterium associated with mortality of white seabass Atractoscion nobilis. Dis Aquat Organ 2000; 43(2): 117-126. http://dx.doi.org/10.3354/dao043117. PMid:11145452.
http://dx.doi.org/10.3354/dao043117...
). The rickettsiosis were found to be especially important in salmon farms, where high mortality was observed (Branson & Diaz-Munoz, 1991Branson EJ, Diaz-Munoz DN. Description of a new disease condition occurring in farmed coho salmon, Oncorhynchus ksiutch (Walbaum), in South America. J Fish Dis 1991; 14(2): 147-156. http://dx.doi.org/10.1111/j.1365-2761.1991.tb00585.x.
http://dx.doi.org/10.1111/j.1365-2761.19...
; Chern & Chao, 1994Chern RS, Chao CB. Outbreaks of a disease caused by rickettsia-like organism in cultured tilapias in Taiwan. Fish Pathol 1994; 29(2): 61-71. http://dx.doi.org/10.3147/jsfp.29.61.
http://dx.doi.org/10.3147/jsfp.29.61...
; Corbeil et al., 2005Corbeil S, Hyatt AD, Crane MSJ. Characterisation of an emerging rickettsia-like organism in Tasmania farmed Atlantic salmon Salmo salar. Dis Aquat Organ 2005; 64(1): 37-44. http://dx.doi.org/10.3354/dao064037. PMid:15900686.
http://dx.doi.org/10.3354/dao064037...
; Cusack et al., 2002Cusack RR, Groman DB, Jones SRM. Rickettsial infection in farmed Atlantic salmon in eastern Canada. Can Vet J 2002; 43(6): 435-440. PMid:12058568.; Fryer et al., 1990Fryer JL, Lannan CN, Garcés LH, Larenas JJ, Smith PA. Isolation of a rickettsiales-like organism from diseased coho salmon (Oncorhynchus kisutch) in Chile. Fish Pathol 1990; 25(2): 107-114. http://dx.doi.org/10.3147/jsfp.25.107.
http://dx.doi.org/10.3147/jsfp.25.107...
; Guo et al., 2004Guo Q, Jia W, Han X, Cai T, Gong X, Sun X. Rickettsia-like organism infection in a freshwater cultured fish Ophiocephalus argus C. in China. J Progr Nat Sci 2004; 14(5): 417-422. http://dx.doi.org/10.1080/10020070412331343711.
http://dx.doi.org/10.1080/10020070412331...
).

These prokaryotic microorganisms cause chronic systemic infections associated with internal and external lesions. Rickettsia-infected fish show lethargic and anorexic behavior, an enlarged abdominal cavity and lesions in various tissues and organs such as the liver, swim bladder and epithelial and muscle tissues, among others. They may also cause epithelial hyperplasia, which results in fusion of the gill lamellae (Branson & Diaz-Munoz, 1991Branson EJ, Diaz-Munoz DN. Description of a new disease condition occurring in farmed coho salmon, Oncorhynchus ksiutch (Walbaum), in South America. J Fish Dis 1991; 14(2): 147-156. http://dx.doi.org/10.1111/j.1365-2761.1991.tb00585.x.
http://dx.doi.org/10.1111/j.1365-2761.19...
; Chern & Chao, 1994Chern RS, Chao CB. Outbreaks of a disease caused by rickettsia-like organism in cultured tilapias in Taiwan. Fish Pathol 1994; 29(2): 61-71. http://dx.doi.org/10.3147/jsfp.29.61.
http://dx.doi.org/10.3147/jsfp.29.61...
).

Human infections caused by ingestion or handling of Rickettsia-infected fish have frequently been reported (Lu et al., 2019Lu M, Li F, Liao Y, Shen J-J, Xu J-M, Chen YZ, et al. Epidemiology and diversity of Rickettsiales Bacteria in humans and animals in Jiangsu and Jiangxi provinces, China. Sci Rep 2019; 9(1): 13176. http://dx.doi.org/10.1038/s41598-019-49059-3. PMid:31511528.
http://dx.doi.org/10.1038/s41598-019-490...
; Novotny et al., 2004Novotny L, Dvorska L, Lorencova A, Beran V, Pavlik I. Fish: A potential source of bacterial pathogens for human beings. Vet Med Czech 2004; 49(9): 343-358. http://dx.doi.org/10.17221/5715-VETMED.
http://dx.doi.org/10.17221/5715-VETMED...
; Shotts, 1987Shotts EB Jr. Bacterial diseases of fish associated with human health. Vet Clin North Am Small Anim Pract 1987; 17(1): 241-247. http://dx.doi.org/10.1016/S0195-5616(87)50615-5. PMid:3551308.
http://dx.doi.org/10.1016/S0195-5616(87)...
).

Prokaryotic parasites have most frequently been described infecting the cytoplasm (Azevedo, 1993Azevedo C. Occurrence of an unusual branchial mycoplasma-like infection in cockle Cerastoderma edule (Mollusca, Bivalvia). Dis Aquat Organ 1993; 16: 55-59. http://dx.doi.org/10.3354/dao016055.
http://dx.doi.org/10.3354/dao016055...
; Cusack et al., 2002Cusack RR, Groman DB, Jones SRM. Rickettsial infection in farmed Atlantic salmon in eastern Canada. Can Vet J 2002; 43(6): 435-440. PMid:12058568.; Guo et al., 2004Guo Q, Jia W, Han X, Cai T, Gong X, Sun X. Rickettsia-like organism infection in a freshwater cultured fish Ophiocephalus argus C. in China. J Progr Nat Sci 2004; 14(5): 417-422. http://dx.doi.org/10.1080/10020070412331343711.
http://dx.doi.org/10.1080/10020070412331...
) and nuclei of eukaryotic hosts (Azevedo, 1989Azevedo C. Fine structure of endonucleobiotic bacteria in gill epithelium of Ruditapes decussatus. Mar Biol 1989; 100(3): 339-341. http://dx.doi.org/10.1007/BF00391149.
http://dx.doi.org/10.1007/BF00391149...
), or living in association with other prokaryotic cells (Azevedo & Villalba, 1991Azevedo C, Villalba A. Extracellular giant rickettsiae associated with bacteria in the gill of Crassostrea gigas (Mollusca, Bivalvia). J Invertebr Pathol 1991; 58(1): 75-81. http://dx.doi.org/10.1016/0022-2011(91)90164-L. PMid:1885924.
http://dx.doi.org/10.1016/0022-2011(91)9...
). They may be pathogenic and lethal (Austin & Austin, 2007Austin B, Austin DA. Bacterial fish pathogens. diseases of farmed and wild fish. 4th ed. United Kingdom: Springer-Praxis Publishing; 2007. https://doi.org/10.1007/978-1-4020-6069-4.
https://doi.org/10.1007/978-1-4020-6069-...
; Chen et al., 2000Chen MF, Yun S, Marty GD, McDowell TS, House ML, Appersen JA, et al. A Piscirickettsia salmonis-like bacterium associated with mortality of white seabass Atractoscion nobilis. Dis Aquat Organ 2000; 43(2): 117-126. http://dx.doi.org/10.3354/dao043117. PMid:11145452.
http://dx.doi.org/10.3354/dao043117...
; Mauel et al., 2003Mauel MJ, Miller DL, Frazier K, Liggett AD, Styer L, Montgomery-Brock D, et al. Characterization of Piscirickettsiosis-like disease in Hawaiian tilapia. Dis Aquat Organ 2003; 53(3): 249-255. http://dx.doi.org/10.3354/dao053249. PMid:12691196.
http://dx.doi.org/10.3354/dao053249...
; Toranzo et al., 2005Toranzo AE, Magariños B, Romalde JL. A review of the main bacterial fish diseases in mariculture systems. Aquaculture 2005; 246(1-4): 37-61. http://dx.doi.org/10.1016/j.aquaculture.2005.01.002.
http://dx.doi.org/10.1016/j.aquaculture....
), and are considered to be obligate parasite (Austin & Austin, 2007Austin B, Austin DA. Bacterial fish pathogens. diseases of farmed and wild fish. 4th ed. United Kingdom: Springer-Praxis Publishing; 2007. https://doi.org/10.1007/978-1-4020-6069-4.
https://doi.org/10.1007/978-1-4020-6069-...
).

The fish species Archosargus probatocephalus (Walbaum, 1792), commonly known as the “sargo” or sheepshead seabream, belongs to the family Sparidae of the order Perciformes, and has wide distribution, ranging from Nova Scotia (Canada) to Brazil (Adams et al., 2018Adams GD, Leaf RT, Ballenger JC, Arnott SA, McDonough CJ. Spatial variability in the growth of Sheepshead (Archosargus probatocephalus) in the southeast US: implications for assessment and management. Fish Res 2018; 206: 35-43. http://dx.doi.org/10.1016/j.fishres.2018.04.023.
http://dx.doi.org/10.1016/j.fishres.2018...
). It is considered to be a species with high potential for aquaculture because of its tolerance to wide temperature ranges, its euryhaline and omnivorous nature and the excellent quality of its meat (Rojas-Castañeda et al., 2017Rojas-Castañeda S, González-Reynoso L, Platas-Rosado DE, Hernández-Arzaba JC, Lango-Reynoso F, Castañeda-Chávez MR, et al. Avances del sargo Archosargus probatocephalus (WALBAUM, 1792) en la acuicultura como respuesta al cambio climático. Rev Iberoam Boecon Cambio Clim 2017; 3(5): 674-679. http://dx.doi.org/10.5377/ribcc.v3i5.5939.
http://dx.doi.org/10.5377/ribcc.v3i5.593...
).

Several studies have suggested that rickettsial species and Rickettsia-like organisms (RLOs) are pathogenic and capable of causing the death of their hosts (Almendras & Fuentealba, 1997Almendras FE, Fuentealba IC. Salmonid rickettsial septicemia caused by Piscirickettsia salmonis: a review. Dis Aquat Organ 1997; 29(2): 137-144. http://dx.doi.org/10.3354/dao029137.
http://dx.doi.org/10.3354/dao029137...
; Yuksel et al., 2006Yuksel SA, Thompson KD, Adams OA. Rickettsial infections of fish. Turk J Fish Aquat Sci 2006; 6: 63-78.; Rozas & Enríquez, 2014Rozas M, Enríquez R. Piscirickettsiosis and Piscirickettsia salmonis in fish: a review. J Fish Dis 2014; 37(3): 163-188. http://dx.doi.org/10.1111/jfd.12211. PMid:24279295.
http://dx.doi.org/10.1111/jfd.12211...
).

The aim of this paper was to describe the ultrastructure of intracytoplasmic prokaryotic cells that cause damage to the organization of the gill cells of Archosargus probatocephalus. These cells were morphologically identified as belonging to the group of RLOs and were found in a survey on microparasites of the gill tissues of a commercially important teleost in Brazil. This formed the first description of these cells in Brazil.

Methodology

Four adult specimens of the sheepshead seabream Archosargus probatocephalus (Brazilian common name “sargo or sargo-de-dente”), were not breeding, with lengths between 15 and 25 cm, were collected from the estuary of the Ipioquinha River (9° 29' S / 35° 34' W), a river partially preserved near the city of Maceió (Alagoas), Brazil, in June and August 2019. They were transported to the aquaculture laboratory of the Agrarian Sciences Center of the Federal University of Alagoas, where biometrics and dissection were performed. Collections were carried out under license number 56475-1, of November 15, 2016, renewed on December 8, 2019 MMA of Brazil.

Light microscopy (LM) and transmission electron microscopy (TEM)

Small fragments of tissues from different organs were checked under a light microscope, to detect any microparasites that might have been present. Small cysts were observed in the gills of a single specimen. The infected material was photographed under this microscope and was then processed for ultrastructural observations.

For TEM, infected fragments of gill tissue were fixed in 4-5% glutaraldehyde in 0.2 M sodium cacodylate buffer (pH 7.2-7.4) for 10-12 h. They were then washed overnight in the same buffer and postfixed with 2% osmium tetroxide in the same buffer for 3 h. All these steps were done at 4 °C. This was followed by dehydration through an ascending ethanol and propylene oxide series and embedding in Epon to form blocks. Semithin sections (~1 µm thick) were stained with methylene blue-Azur II. Ultrathin sections were double-contrasted with uranyl acetate and lead citrate, and were observed using a TEM (JEOL 100CXII; JEOL Optical, Tokyo, Japan), operated at 60 kV.

Results

A single specimen displayed infection by myxosporean species contained within cysts, which measured up to 125 µm and appeared located in the peripheral region of the gill filaments (Figure 1A). The cysts were surrounded by several layers of epithelial cells, some of which displayed cytoplasmic vacuoles containing small dense bodies that could not be identified in semithin sections (Figure 1A). TEM observations revealed that the ultrastructural aspects of these small bodies were congruent with the morphological features of prokaryotic organisms, namely RLOs (Figure 1BF).

Figure 1
Light and transmission electron microscopy aspects of gill epithelial cells of the teleost Archosargus probatocephalus. Some of these cells presented generally a single large cytoplasmic vacuole containing Rickettsia-like organisms (RLOs). A - Semithin section of a cyst (C) containing myxospores surrounded by different gill cells (GC), infected by RLOs within vacuoles that were hardly observed in LM; B - Ultrathin section showing the periphery of the gill, where an infected host cell (HC) with a vacuole (V) containing some Rickettsia-like cells are present. Near the vacuole (V), some cellular material seems lysed (Ly); C - Ultrastructural appearance of an infected host cell (HC) located near to the periphery of the gill, in which the nucleus (Nu) is in contact with the vacuole (V) containing the RLOs. The HC shows high-grade of lysis (*); D - Ultrastructural appearance of the cytoplasm of a host cell containing a vacuole (V) with several pleomorphic RLOs. The cytoplasm of the host cell and the membrane of the vacuole show advanced stages of degradation (*). Partial portion of the nucleus (Nu) showing the closed contact with the vacuole content; E - Ultrastructural details of a host cell (HC) showing two type of vacuoles. The biggest containing several RLOs (V), while the smallest one (V*) appeared empty of RLOs. The vacuole membrane and the nucleus (*) show degraded aspects. F - Ultrastructural details showing some RLOs within the vacuole (V) that seems well preserved, while the membrane and the surrounding cytoplasm of the host cell appears highly lysed (*).

The RLOs were found in variable numbers per section (most frequently 5-7) (Figure 1B, F). Serial ultrathin sections showed variable numbers of RLOs (up to 11) located within several voluminous vacuoles of the infected host cells (Figure 1CE). These vacuoles were more frequently located at the periphery of the epithelial cells in which the cysts were located (Figure 1B, C). Most of them displayed a degraded membrane and presented various aspects of rupture and RLO release (Figure 1C - F). The cytoplasm of the host cell surrounding the vacuole membrane also showed an appearance of severe lysis (Figure 1CE).

The RLOs were pleomorphic, and their DNA appeared randomly distributed in the internal granular cytoplasm, forming a reticular nucleoid without a nuclear envelope (Figure 1DF). The nuclear envelope and the nucleoplasm of the host cells displayed typical organization (Figure 1 CE).

In these observations, it was not possible to detect morphological aspects that would suggest that the RLOs had influenced mortality.

Discussion

Intracellular prokaryotes have frequently been described in different aquatic species and in several geographical locations, as: Ruditapes decussatus (Mollusca, Bivalvia), collected in Portugal (Azevedo, 1989Azevedo C. Fine structure of endonucleobiotic bacteria in gill epithelium of Ruditapes decussatus. Mar Biol 1989; 100(3): 339-341. http://dx.doi.org/10.1007/BF00391149.
http://dx.doi.org/10.1007/BF00391149...
); Venerupis rhomboides, from Spain (Villalba et al., 1999Villalba A, Carballal MJ, López C, Cabada A, Corral L, Azevedo C. Branchial rickettsia-like infection associated with clam Venerupis rhomboides mortality. Dis Aquat Organ 1999; 36(1): 53-60. http://dx.doi.org/10.3354/dao036053.
http://dx.doi.org/10.3354/dao036053...
); juvenile Atractoscion nobilis, collected in the California (USA) (Chen et al., 2000Chen MF, Yun S, Marty GD, McDowell TS, House ML, Appersen JA, et al. A Piscirickettsia salmonis-like bacterium associated with mortality of white seabass Atractoscion nobilis. Dis Aquat Organ 2000; 43(2): 117-126. http://dx.doi.org/10.3354/dao043117. PMid:11145452.
http://dx.doi.org/10.3354/dao043117...
); Mytella guyanensis from, Bahia (Brazil) (Ceuta & Boehs, 2012Ceuta LO, Boehs G. Parasites in the mangrove mussel Mytella guyanensis (Bivalvia: Mytilidae) in Camamu Bay, Bahia, Brazil. Braz J Biol 2012; 72(3): 421-427. http://dx.doi.org/10.1590/S1519-69842012000300002. PMid:22990810.
http://dx.doi.org/10.1590/S1519-69842012...
); Crassostrea gasar, cultivated in northeastern Brazil (Silva et al., 2015Silva PM, Scardua MP, Vieira CB, Alves AC, Dungan CF. Survey of pathologies in Crassostrea gasar (Adanson, 1757) oysters from cultured and wild populations in the São Francisco estuary, Sergipe, Northeast Brazil. J Shellfish Res 2015; 34(2): 289-296. http://dx.doi.org/10.2983/035.034.0210.
http://dx.doi.org/10.2983/035.034.0210...
) and Oncorhynchus tshawytscha, from farms in New Zealand (Brosnahan et al., 2019Brosnahan CL, Munday JS, Ha HJ, Preece M, Jones JB. New Zealand rickettsia‐like organism (NZ‐RLO) and Tenacibaculum maritimum: distribution and phylogeny in farmed Chinook salmon (Oncorhynchus tshawytscha). J Fish Dis 2019; 42(1): 85-95. http://dx.doi.org/10.1111/jfd.12909. PMid:30411368.
http://dx.doi.org/10.1111/jfd.12909...
).

The ultrastructural characteristics of the prokaryotic cells observed in this study, namely their pleomorphic shape and lack of mitochondria and nuclear envelope, suggested that they belonged to the order Rickettsiales, genus Rickettsia. They are described here as Rickettsia-like organisms (RLOs). The morphological characteristics that identify these RLOs have already been described in numerous reports (Azevedo & Villalba, 1991Azevedo C, Villalba A. Extracellular giant rickettsiae associated with bacteria in the gill of Crassostrea gigas (Mollusca, Bivalvia). J Invertebr Pathol 1991; 58(1): 75-81. http://dx.doi.org/10.1016/0022-2011(91)90164-L. PMid:1885924.
http://dx.doi.org/10.1016/0022-2011(91)9...
; Cusack et al., 2002Cusack RR, Groman DB, Jones SRM. Rickettsial infection in farmed Atlantic salmon in eastern Canada. Can Vet J 2002; 43(6): 435-440. PMid:12058568.; Guo et al., 2004Guo Q, Jia W, Han X, Cai T, Gong X, Sun X. Rickettsia-like organism infection in a freshwater cultured fish Ophiocephalus argus C. in China. J Progr Nat Sci 2004; 14(5): 417-422. http://dx.doi.org/10.1080/10020070412331343711.
http://dx.doi.org/10.1080/10020070412331...
). The ultrastructure of the outer membrane of the cell wall and cytoplasmic membrane further revealed them to be Gram-negative. This information was not given in most previous descriptions (Fryer & Lannan, 1994Fryer JL, Lannan CN. Rickettsial and chlamydial infections of freshwater and marine fishes, bivalves, and crustaceans. Zool Stud 1994; 33(2): 95-107.), with the exception of Fryer & Hedrick (2003)Fryer JL, Hedrick RP. Piscirickettsia salmonis: a Gram‐negative intracellular bacterial pathogen of fish. J Fish Dis 2003; 26(5): 251-262. http://dx.doi.org/10.1046/j.1365-2761.2003.00460.x. PMid:12962234.
http://dx.doi.org/10.1046/j.1365-2761.20...
.

This was the first description of an intracellular prokaryotic RLO from this Brazilian host fish (Archosargus probatocephalus). This seems to be a situation that has frequently been encountered, with occasional reports of numerous eukaryotic cells in aquatic species in different taxonomic groups. It also seems to occur more frequently as an intracytoplasmic infection (Azevedo, 1993Azevedo C. Occurrence of an unusual branchial mycoplasma-like infection in cockle Cerastoderma edule (Mollusca, Bivalvia). Dis Aquat Organ 1993; 16: 55-59. http://dx.doi.org/10.3354/dao016055.
http://dx.doi.org/10.3354/dao016055...
; Azevedo et al., 2005Azevedo C, Padovan I, Corral L, Padovan P. Ultrastructural description of an unidentified apicomplexan oocyst containing bacteria-like hyperparasites in the gill of Crassostrea rizophorae. Dis Aquat Organ 2005; 65(2): 153-157. http://dx.doi.org/10.3354/dao065153. PMid:16060268.
http://dx.doi.org/10.3354/dao065153...
), than as an intranuclear infection (Azevedo, 1989Azevedo C. Fine structure of endonucleobiotic bacteria in gill epithelium of Ruditapes decussatus. Mar Biol 1989; 100(3): 339-341. http://dx.doi.org/10.1007/BF00391149.
http://dx.doi.org/10.1007/BF00391149...
). In another report, a giant rickettsial organism associated with bacteria in the molluscan gills of Crassostrea gigas caused host mortality (Azevedo & Villalba, 1991Azevedo C, Villalba A. Extracellular giant rickettsiae associated with bacteria in the gill of Crassostrea gigas (Mollusca, Bivalvia). J Invertebr Pathol 1991; 58(1): 75-81. http://dx.doi.org/10.1016/0022-2011(91)90164-L. PMid:1885924.
http://dx.doi.org/10.1016/0022-2011(91)9...
).

Intracellular prokaryotic microorganisms have never before been reported from the sheepshead seabream. This fish species is distributed along large proportions of the North and South American Atlantic coasts (Rojas-Castañeda et al., 2017Rojas-Castañeda S, González-Reynoso L, Platas-Rosado DE, Hernández-Arzaba JC, Lango-Reynoso F, Castañeda-Chávez MR, et al. Avances del sargo Archosargus probatocephalus (WALBAUM, 1792) en la acuicultura como respuesta al cambio climático. Rev Iberoam Boecon Cambio Clim 2017; 3(5): 674-679. http://dx.doi.org/10.5377/ribcc.v3i5.5939.
http://dx.doi.org/10.5377/ribcc.v3i5.593...
). Thus, the present study constitutes the first description of an intracytoplasmic prokaryote in this fish species, and specifically from a geographical region where it is commercially valuable for human consumption.

The lack of data in the literature with regard to vacuole-forming intracytoplasmic infections in fish hosts hampers recognition of the degree of tissue degradation that may result from these types of infections, along with detailed assessment of the histopathological effects of RLOs. Considering that the present study resulted from a chance finding during the course of a myxozoan survey conducted on Archosargus probatocephalus (work in progress), we are unable to say whether the RLOs described here can increase host mortality. Nevertheless, a previous study showed that infection by RLOs may occur through weakened host immunity, as a result of abiotic changes to the aquatic environment (Soares et al., 2013Soares S, Murray AG, Crumlish M, Turnbull JF, Green DM. Factors affecting variation in mortality of marine Atlantic salmon Salmo salar in Scotland. Dis Aquat Organ 2013; 103(2): 101-109. http://dx.doi.org/10.3354/dao02562. PMid:23548360.
http://dx.doi.org/10.3354/dao02562...
).

It is well known that various species of invertebrates, and especially arthropods and bivalves, act as transmission vectors for RLOs. However, no information is available regarding the possibility that infected fish might be active transmitters of rickettsiosis.

Our results do not allow any suggestions regarding the mode of infection or development of these prokaryotic parasites within the host. The way in which the RLOs were organized, with evidence of vacuole membrane rupture and degradation of host cytoplasm, suggests that they possibly had pathogenic activity.

Little is known about the mechanisms through which RLOs penetrate into host cells (Austin & Austin, 2007Austin B, Austin DA. Bacterial fish pathogens. diseases of farmed and wild fish. 4th ed. United Kingdom: Springer-Praxis Publishing; 2007. https://doi.org/10.1007/978-1-4020-6069-4.
https://doi.org/10.1007/978-1-4020-6069-...
). Some studies have suggested that food vacuoles (phagosomes) may be a possible means through which RLOs enter into host cells (Silverman et al., 1992Silverman DJ, Santucci LA, Meyers N, Sekeyova Z. Penetration of host cells by Rickettsia rickettsii appears to be mediated by a phospholipase of rickettsial origin. Infect Immun 1992; 60(7): 2733-2740. http://dx.doi.org/10.1128/IAI.60.7.2733-2740.1992. PMid:1612741.
http://dx.doi.org/10.1128/IAI.60.7.2733-...
). Others have described action mediated by phospholipase, i.e. “induced phagocytosis” (Silverman et al., 1992Silverman DJ, Santucci LA, Meyers N, Sekeyova Z. Penetration of host cells by Rickettsia rickettsii appears to be mediated by a phospholipase of rickettsial origin. Infect Immun 1992; 60(7): 2733-2740. http://dx.doi.org/10.1128/IAI.60.7.2733-2740.1992. PMid:1612741.
http://dx.doi.org/10.1128/IAI.60.7.2733-...
). Occurrences of dissemination to neighboring cells, were reported by Weddle & Agaisse (2018)Weddle E, Agaisse H. Principles of intracellular bacterial pathogen spread from cell to cell. PLoS Pathog 2018; 14(12): e1007380. http://dx.doi.org/10.1371/journal.ppat.1007380. PMid:30543716.
http://dx.doi.org/10.1371/journal.ppat.1...
, who observed that RLOs used the cytoskeleton of the host cell to move from infected cells and project to adjacent cells.

Experimental results from artificial infestation of fish with Rickettsia have suggested that cell penetration occurs through the skin and gills (Smith et al., 1999Smith PA, Pizarro P, Ojeda P, Contreras J, Oyanedel S, Larenas J. Routes of entry of Piscirickettsia salmonis in rainbow trout Oncorhynchus mykiss. Dis Aquat Organ 1999; 37(3): 165-172. http://dx.doi.org/10.3354/dao037165. PMid:10546046.
http://dx.doi.org/10.3354/dao037165...
, 2004Smith PA, Rojas ME, Guajardo A, Contreras J, Morales A, Larenas J. Experimental infection of coho salmon Oncorhynchus kisutch by exposure of skin, gills and intestine with Piscirickettsia salmonis. Dis Aquat Organ 2004; 61(1-2): 53-57. http://dx.doi.org/10.3354/dao061053. PMid:15584410.
http://dx.doi.org/10.3354/dao061053...
). Some authors have suggested that occurrences of rickettsiosis may result from biotic factors such as pathogens and abiotic causes such as pollution (Austin & Austin, 2007Austin B, Austin DA. Bacterial fish pathogens. diseases of farmed and wild fish. 4th ed. United Kingdom: Springer-Praxis Publishing; 2007. https://doi.org/10.1007/978-1-4020-6069-4.
https://doi.org/10.1007/978-1-4020-6069-...
). Considering that, in the present study, RLOs were found contained within cytoplasmic vacuoles located on the periphery of gill epithelial cells, our observations support the idea that RLO penetration occurs mainly through this organ. In addition, the high number of RLOs contained in the same vacuole possibly suggests that penetration of host cells is accompanied by occurrences of cell division, from a single penetrating RLO.

Further detailed observations are needed in order to better understand the evolution of RLOs, which will help in the future to elucidate the mechanisms of host infection, life cycle, transmission and pathogenicity.

  • How to cite: Silva TJ, Casal G, Soares EC, Rocha S, Santos EL, Oliveira E, et al. Ultrastructure of intracytoplasmic Rickettsia-like infection of the gills of the teleost Archosargus probatocephalus (Sparidae) in northeastern Brazil. Braz J Vet Parasitol 2020; 29(3): e010020. https://doi.org/10.1590/S1984-29612020067

References

  • Adams GD, Leaf RT, Ballenger JC, Arnott SA, McDonough CJ. Spatial variability in the growth of Sheepshead (Archosargus probatocephalus) in the southeast US: implications for assessment and management. Fish Res 2018; 206: 35-43. http://dx.doi.org/10.1016/j.fishres.2018.04.023
    » http://dx.doi.org/10.1016/j.fishres.2018.04.023
  • Almendras FE, Fuentealba IC. Salmonid rickettsial septicemia caused by Piscirickettsia salmonis: a review. Dis Aquat Organ 1997; 29(2): 137-144. http://dx.doi.org/10.3354/dao029137
    » http://dx.doi.org/10.3354/dao029137
  • Athanassopoulou F, Karagouni E. Rickettsia-like organisms (R.L.O.) infections of fin-fish. J Hell Vet Med Soc 2004; 55(2): 165-173. http://dx.doi.org/10.12681/jhvms.15188
    » http://dx.doi.org/10.12681/jhvms.15188
  • Austin B, Austin DA. Bacterial fish pathogens. diseases of farmed and wild fish 4th ed. United Kingdom: Springer-Praxis Publishing; 2007. https://doi.org/10.1007/978-1-4020-6069-4
    » https://doi.org/10.1007/978-1-4020-6069-4
  • Azevedo C, Padovan I, Corral L, Padovan P. Ultrastructural description of an unidentified apicomplexan oocyst containing bacteria-like hyperparasites in the gill of Crassostrea rizophorae. Dis Aquat Organ 2005; 65(2): 153-157. http://dx.doi.org/10.3354/dao065153 PMid:16060268.
    » http://dx.doi.org/10.3354/dao065153
  • Azevedo C, Villalba A. Extracellular giant rickettsiae associated with bacteria in the gill of Crassostrea gigas (Mollusca, Bivalvia). J Invertebr Pathol 1991; 58(1): 75-81. http://dx.doi.org/10.1016/0022-2011(91)90164-L PMid:1885924.
    » http://dx.doi.org/10.1016/0022-2011(91)90164-L
  • Azevedo C. Fine structure of endonucleobiotic bacteria in gill epithelium of Ruditapes decussatus. Mar Biol 1989; 100(3): 339-341. http://dx.doi.org/10.1007/BF00391149
    » http://dx.doi.org/10.1007/BF00391149
  • Azevedo C. Occurrence of an unusual branchial mycoplasma-like infection in cockle Cerastoderma edule (Mollusca, Bivalvia). Dis Aquat Organ 1993; 16: 55-59. http://dx.doi.org/10.3354/dao016055
    » http://dx.doi.org/10.3354/dao016055
  • Birkbecka TH, Ringøb E. Pathogenesis and the gastrointestinal tract of growing fish. Biol Grow Anim 2005; 2: 208-234. http://dx.doi.org/10.1016/S1877-1823(09)70043-8
    » http://dx.doi.org/10.1016/S1877-1823(09)70043-8
  • Bower SM, McGladdery SE, Price IM. Synopsis of infection diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 1994; 4: 1-199. http://dx.doi.org/10.1016/0959-8030(94)90028-0
    » http://dx.doi.org/10.1016/0959-8030(94)90028-0
  • Branson EJ, Diaz-Munoz DN. Description of a new disease condition occurring in farmed coho salmon, Oncorhynchus ksiutch (Walbaum), in South America. J Fish Dis 1991; 14(2): 147-156. http://dx.doi.org/10.1111/j.1365-2761.1991.tb00585.x
    » http://dx.doi.org/10.1111/j.1365-2761.1991.tb00585.x
  • Brosnahan CL, Munday JS, Ha HJ, Preece M, Jones JB. New Zealand rickettsia‐like organism (NZ‐RLO) and Tenacibaculum maritimum: distribution and phylogeny in farmed Chinook salmon (Oncorhynchus tshawytscha). J Fish Dis 2019; 42(1): 85-95. http://dx.doi.org/10.1111/jfd.12909 PMid:30411368.
    » http://dx.doi.org/10.1111/jfd.12909
  • Ceuta LO, Boehs G. Parasites in the mangrove mussel Mytella guyanensis (Bivalvia: Mytilidae) in Camamu Bay, Bahia, Brazil. Braz J Biol 2012; 72(3): 421-427. http://dx.doi.org/10.1590/S1519-69842012000300002 PMid:22990810.
    » http://dx.doi.org/10.1590/S1519-69842012000300002
  • Chen MF, Yun S, Marty GD, McDowell TS, House ML, Appersen JA, et al. A Piscirickettsia salmonis-like bacterium associated with mortality of white seabass Atractoscion nobilis. Dis Aquat Organ 2000; 43(2): 117-126. http://dx.doi.org/10.3354/dao043117 PMid:11145452.
    » http://dx.doi.org/10.3354/dao043117
  • Chern RS, Chao CB. Outbreaks of a disease caused by rickettsia-like organism in cultured tilapias in Taiwan. Fish Pathol 1994; 29(2): 61-71. http://dx.doi.org/10.3147/jsfp.29.61
    » http://dx.doi.org/10.3147/jsfp.29.61
  • Corbeil S, Hyatt AD, Crane MSJ. Characterisation of an emerging rickettsia-like organism in Tasmania farmed Atlantic salmon Salmo salar. Dis Aquat Organ 2005; 64(1): 37-44. http://dx.doi.org/10.3354/dao064037 PMid:15900686.
    » http://dx.doi.org/10.3354/dao064037
  • Cusack RR, Groman DB, Jones SRM. Rickettsial infection in farmed Atlantic salmon in eastern Canada. Can Vet J 2002; 43(6): 435-440. PMid:12058568.
  • Fryer JL, Hedrick RP. Piscirickettsia salmonis: a Gram‐negative intracellular bacterial pathogen of fish. J Fish Dis 2003; 26(5): 251-262. http://dx.doi.org/10.1046/j.1365-2761.2003.00460.x PMid:12962234.
    » http://dx.doi.org/10.1046/j.1365-2761.2003.00460.x
  • Fryer JL, Lannan CN, Garcés LH, Larenas JJ, Smith PA. Isolation of a rickettsiales-like organism from diseased coho salmon (Oncorhynchus kisutch) in Chile. Fish Pathol 1990; 25(2): 107-114. http://dx.doi.org/10.3147/jsfp.25.107
    » http://dx.doi.org/10.3147/jsfp.25.107
  • Fryer JL, Lannan CN, Giovannoni SJ, Wood ND. Piscirickettsia salmonis gen. nov., sp. nov., the causative agent of an epizootic disease in salmonid fishes. Int J Syst Bacteriol 1992; 42(1): 120-126. http://dx.doi.org/10.1099/00207713-42-1-120 PMid:1371057.
    » http://dx.doi.org/10.1099/00207713-42-1-120
  • Fryer JL, Lannan CN. Rickettsial and chlamydial infections of freshwater and marine fishes, bivalves, and crustaceans. Zool Stud 1994; 33(2): 95-107.
  • Goggin GL, Lester RJG. Rickettsiales-like infection in the gill in Tridacna crocea from Great Barrier Reef. J Invertebr Pathol 1990; 56(1): 135-138. http://dx.doi.org/10.1016/0022-2011(90)90156-Z PMid:2376662.
    » http://dx.doi.org/10.1016/0022-2011(90)90156-Z
  • Guo Q, Jia W, Han X, Cai T, Gong X, Sun X. Rickettsia-like organism infection in a freshwater cultured fish Ophiocephalus argus C. in China. J Progr Nat Sci 2004; 14(5): 417-422. http://dx.doi.org/10.1080/10020070412331343711
    » http://dx.doi.org/10.1080/10020070412331343711
  • Lu M, Li F, Liao Y, Shen J-J, Xu J-M, Chen YZ, et al. Epidemiology and diversity of Rickettsiales Bacteria in humans and animals in Jiangsu and Jiangxi provinces, China. Sci Rep 2019; 9(1): 13176. http://dx.doi.org/10.1038/s41598-019-49059-3 PMid:31511528.
    » http://dx.doi.org/10.1038/s41598-019-49059-3
  • Mauel MJ, Miller DL, Frazier K, Liggett AD, Styer L, Montgomery-Brock D, et al. Characterization of Piscirickettsiosis-like disease in Hawaiian tilapia. Dis Aquat Organ 2003; 53(3): 249-255. http://dx.doi.org/10.3354/dao053249 PMid:12691196.
    » http://dx.doi.org/10.3354/dao053249
  • Mauel MJ, Soto E, Moralis J, Hawke J. A piscirickettsiosis-like syndrome in cultured Nile tilapia in Latin America with a Francisella spp. as the pathogenic agent. J Aquat Anim Health 2007; 19(1): 27-34. http://dx.doi.org/10.1577/H06-025.1 PMid:18236629.
    » http://dx.doi.org/10.1577/H06-025.1
  • Miquel A, Müller I, Ferrer P, Valenzuela PDT, Burzio LO. Immunoresponse of Coho salmon immunized with a gene expression library from Piscirickettsia salmonis. Biol Res 2003; 36(3-4): 313-323. http://dx.doi.org/10.4067/S0716-97602003000300004 PMid:14631865.
    » http://dx.doi.org/10.4067/S0716-97602003000300004
  • Molloy DP, Giamberini L, Morado JF, Fokin SI, Laruelle F. Characterization of intracytoplasmic prokaryote infections in Dreissena sp. (Bivalvia: dreissenidae). Dis Aquat Organ 2001; 44(3): 203-216. http://dx.doi.org/10.3354/dao044203 PMid:11383568.
    » http://dx.doi.org/10.3354/dao044203
  • Novotny L, Dvorska L, Lorencova A, Beran V, Pavlik I. Fish: A potential source of bacterial pathogens for human beings. Vet Med Czech 2004; 49(9): 343-358. http://dx.doi.org/10.17221/5715-VETMED
    » http://dx.doi.org/10.17221/5715-VETMED
  • Palmer R, Ruttledge M, Callanan K, Drinan E. A Piscirickettsiosis-like disease in farmed Atlantic salmon in Ireland-isolation of the agent. Bull Eur Assoc Fish Pathol 1996; 17(2): 68-72.
  • Rojas-Castañeda S, González-Reynoso L, Platas-Rosado DE, Hernández-Arzaba JC, Lango-Reynoso F, Castañeda-Chávez MR, et al. Avances del sargo Archosargus probatocephalus (WALBAUM, 1792) en la acuicultura como respuesta al cambio climático. Rev Iberoam Boecon Cambio Clim 2017; 3(5): 674-679. http://dx.doi.org/10.5377/ribcc.v3i5.5939
    » http://dx.doi.org/10.5377/ribcc.v3i5.5939
  • Rozas M, Enríquez R. Piscirickettsiosis and Piscirickettsia salmonis in fish: a review. J Fish Dis 2014; 37(3): 163-188. http://dx.doi.org/10.1111/jfd.12211 PMid:24279295.
    » http://dx.doi.org/10.1111/jfd.12211
  • Shotts EB Jr. Bacterial diseases of fish associated with human health. Vet Clin North Am Small Anim Pract 1987; 17(1): 241-247. http://dx.doi.org/10.1016/S0195-5616(87)50615-5 PMid:3551308.
    » http://dx.doi.org/10.1016/S0195-5616(87)50615-5
  • Silva PM, Scardua MP, Vieira CB, Alves AC, Dungan CF. Survey of pathologies in Crassostrea gasar (Adanson, 1757) oysters from cultured and wild populations in the São Francisco estuary, Sergipe, Northeast Brazil. J Shellfish Res 2015; 34(2): 289-296. http://dx.doi.org/10.2983/035.034.0210
    » http://dx.doi.org/10.2983/035.034.0210
  • Silverman DJ, Santucci LA, Meyers N, Sekeyova Z. Penetration of host cells by Rickettsia rickettsii appears to be mediated by a phospholipase of rickettsial origin. Infect Immun 1992; 60(7): 2733-2740. http://dx.doi.org/10.1128/IAI.60.7.2733-2740.1992 PMid:1612741.
    » http://dx.doi.org/10.1128/IAI.60.7.2733-2740.1992
  • Smith PA, Pizarro P, Ojeda P, Contreras J, Oyanedel S, Larenas J. Routes of entry of Piscirickettsia salmonis in rainbow trout Oncorhynchus mykiss. Dis Aquat Organ 1999; 37(3): 165-172. http://dx.doi.org/10.3354/dao037165 PMid:10546046.
    » http://dx.doi.org/10.3354/dao037165
  • Smith PA, Rojas ME, Guajardo A, Contreras J, Morales A, Larenas J. Experimental infection of coho salmon Oncorhynchus kisutch by exposure of skin, gills and intestine with Piscirickettsia salmonis. Dis Aquat Organ 2004; 61(1-2): 53-57. http://dx.doi.org/10.3354/dao061053 PMid:15584410.
    » http://dx.doi.org/10.3354/dao061053
  • Smith PA, Vecchiola IM, Oyanedel S, Garcés LH, Larenas J, Contreras J. Antimicrobial sensitivity of four isolates of Piscirickettsia salmonis. Bull Eur Assoc Fish Pathol 1996; 16: 164-168.
  • Soares S, Murray AG, Crumlish M, Turnbull JF, Green DM. Factors affecting variation in mortality of marine Atlantic salmon Salmo salar in Scotland. Dis Aquat Organ 2013; 103(2): 101-109. http://dx.doi.org/10.3354/dao02562 PMid:23548360.
    » http://dx.doi.org/10.3354/dao02562
  • Toranzo AE, Magariños B, Romalde JL. A review of the main bacterial fish diseases in mariculture systems. Aquaculture 2005; 246(1-4): 37-61. http://dx.doi.org/10.1016/j.aquaculture.2005.01.002
    » http://dx.doi.org/10.1016/j.aquaculture.2005.01.002
  • Turnbull JF. Rickettsias and Chlamydias. In: Inglish V, Roberts RJ, Bromage NR. Bacterial Diseases of Fish Oxford: Willey-Blackwell; 1993. p. 235-254.
  • Villalba A, Carballal MJ, López C, Cabada A, Corral L, Azevedo C. Branchial rickettsia-like infection associated with clam Venerupis rhomboides mortality. Dis Aquat Organ 1999; 36(1): 53-60. http://dx.doi.org/10.3354/dao036053
    » http://dx.doi.org/10.3354/dao036053
  • Weddle E, Agaisse H. Principles of intracellular bacterial pathogen spread from cell to cell. PLoS Pathog 2018; 14(12): e1007380. http://dx.doi.org/10.1371/journal.ppat.1007380 PMid:30543716.
    » http://dx.doi.org/10.1371/journal.ppat.1007380
  • Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM. Evolution and diversity of Rickettsia bacteria. BMC Biol 2009; 7(1): 6. http://dx.doi.org/10.1186/1741-7007-7-6 PMid:19187530.
    » http://dx.doi.org/10.1186/1741-7007-7-6
  • Yuksel SA, Thompson KD, Adams OA. Rickettsial infections of fish. Turk J Fish Aquat Sci 2006; 6: 63-78.

Publication Dates

  • Publication in this collection
    28 Sept 2020
  • Date of issue
    2020

History

  • Received
    28 Apr 2020
  • Accepted
    01 July 2020
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
E-mail: cbpv_rbpv.fcav@unesp.br