New morphological data and molecular diagnostic of Henneguya friderici (Myxozoa: Myxobolidae), a parasite of Leporinus friderici (Osteichthyes: Anostomidae) from southeastern Brazil

Novos dados morfológicos e diagnóstico molecular de Henneguya friderici (Myxozoa: Myxobolidae), parasito de Leporinus friderici (Osteichthyes: Anostomidae) do sudeste do Brasil

Abstract

The myxozoan Henneguya friderici is a parasite of the gills, intestine, kidney and liver of Leporinus friderici, a characiform fish belonging to the family Anostomidae. Forty-two specimens of L. friderici that had been caught in the Mogi Guaçú River, state of São Paulo, were studied. Elongated white plasmodia were found in the gill filaments of 10 host specimens (24%). The mature spores had an ellipsoidal body with polar capsules of equal size and caudal length greater than body length. This study also described 18S rDNA sequencing of H. friderici infecting the gill filaments. This produced a sequence of 1050 bp that demonstrated significant genetic differences with previously described species of Henneguya. Similarity analysis using sequences from species that clustered closest to those produced by this study showed that the species with greatest genetic similarity to H. friderici was H. leporinicola, with 94% similarity.

Keywords:
Myxosporea; Characiformes; 18S rDNA; phylogeny

Resumo

O myxozoa Henneguya friderici é um parasito encontrado nas brânquias, fígado, intestino e rins de Leporinus friderici, (Characiformes: Anastomidae). Foram capturados e examinados quarenta e dois espécimes de L. friderici oriundos do Rio Mogi Guaçú, estado de São Paulo. Cistos alongados e brancos foram encontrados nos filamentos branquiais de 10 (24%) hospedeiros. Os esporos maduros apresentaram o corpo alongado com as cápsulas polares em tamanhos iguais e o comprimento caudal maior do que o comprimento corporal. Com isso, o presente trabalho, descreve o sequenciamento de 1050 pb do gene 18S rDNA de H. friderici infectando os filamentos branquiais, o que demonstrou diferenças genéticas significativas em comparação com espécies previamente descritas de Henneguya. A análise de similaridade utilizando as sequencias de espécies que se agruparam mais próximas às produzidas por este estudo mostrou que a espécie com maior semelhança genética com H. friderici foi H. leporinicola, com 94% de similaridade.

Paravras-chave:
Myxosporea; Characiformes,18S rDNA; filogenia

Introduction

The diversity of known myxozoans has grown greatly since the early work of Kudo (1919). Around 2.200 species have now been described (LOM & DYKOVÁ, 2006) and these represent around 18% of cnidarian species diversity, as far as is currently known (OKAMURA et al., 2015). Henneguya Thélohan, 1892, is one of the most diverse genera of Myxosporea and currently includes more than 200 known and described species (LOM & DYKOVÁ, 2006). This widespread genus includes typical coelozoic and histozoic species and predominantly infects marine and freshwater fish (EIRAS & ADRIANO, 2012).

Currently, more than 44 species of Henneguya are known to infect South America fish (EIRAS, 2002; EIRAS & ADRIANO, 2012; CARRIERO et al., 2013; NALDONI et al., 2014). Of these, around 28 have been found to infect fish species of the order Characiformes.

Identification of the species in this genus, like those in other genera of myxozoans, is based almost exclusively on spore morphology. In the class Myxosporea, morphology has been the main criterion for classification of species (KUDO, 1933; MOLNÁR, 1994). In fact, this method has always failed to identify highly similar species that are found in the same infection site and host and which only have subtle differences in spore structures (YE et al., 2012). Fortunately, this problem has been solved through molecular approaches (SMOTHERS et al., 1994; ANDREE et al., 1999; HOLZER et al., 2004). 18S rDNA is the molecular marker that has most commonly been used for detection, identification and phylogenetic analysis on myxozoans (HOLZER et al., 2006). The difficulties of relying on spore morphology for species identification have led authors to recommend that SSU rDNA sequencing should be included when new species are described (ANDREE et al., 1999; KENT et al., 2001; LOM & DYKOVÁ, 2006).

Leporinus friderici (Bloch, 1794) is a characiform fish belonging to the family Anostomidae that is, popularly known in Brazil as “piau”. It is widely distributed in the Amazon and Paraguay river basins (FROESE & PAULY, 2016). Among the species of Henneguya, only Henneguya friderici (CASAL et al., 2003) has been reported from L. friderici.

Henneguya friderici was found infecting the gills, intestine, kidney and liver of “piau” from an estuarine region of the Amazon River, in the state of Pará, Brazil. Relative organelle preservation occurred in the liver tissue and, in some cases, development of the parasite caused gradual and generalized degeneration in the intestine, gills and kidney (CASAL et al., 2003)

The present paper supplements the original description of H. friderici with new data on morphology and 18S rDNA sequencing on samples from gill filaments of L. friderici from the Mogi Guaçú River, state of São Paulo, Brazil. The new data support the original diagnosis by Casal et al. (2003).

Materials and Methods

Forty-two specimens of L. friderici were caught by local fishermen with nets and hooks in the Mogi Guaçú River near Pirassununga, state of São Paulo, Brazil (21°55’36” S; 47°22’6” W), between January 2014 and January 2016. Gills extracted from the fish were placed in Petri dishes with tap water and were examined for myxozoans using a dissecting microscope. Infected gill filaments were preserved using two different methods: frozen (for spore measurements) and in 95% ethanol (for DNA analysis).

Parasitological examinations were conducted using standard methods with the aid of an optical microscope (Olympus BX51) with differential interference contrast (DIC). Images were captured using a 3.2 mp UC30 digital camera and were analyzed by means of photomicrography software (Cell^D 3.4, Olympus Soft Imaging Solutions GmbH, Germany). At least 30 measurements were made for each relevant spore dimension, following the guidelines of Lom & Arthur (1989).

Gill filaments from three hosts were used for DNA extraction by means of the DNeasy Blood & Tissue Kit, following the manufacturer’s instructions (QIAGEN Inc., California, USA). The polymerase chain reaction (PCR) was performed as described by Whipps et al. (2015) in 50 µl reaction volumes of the Quick-Load Taq 23 Master Mix (New England Biolabs, Ipswich, Massachusetts, USA), with 0.5 µM of each primer and 3 µl of template DNA. A first round of amplification targeting the small subunit (SUU) rDNA was performed using the primers 18E and 18R (WHIPPS et al., 2003), followed by a second round of PCR with 18E and Myxgen2R (KENT et al., 2000) or with 18R and Myxgen3F (KENT et al., 2000). The amplifications were performed in a C1000^TM thermal cycler (BioRad Laboratories, Hercules, California, USA) with initial denaturation at 95 °C for 3 min, followed by 35 cycles of 94 °C for 30 s, 56 °C for 45 s and 68 °C for 90 s, and a final extension at 72 °C for 7 min. Product amplification was evaluated by observation on 1% agarose gel, and the remainder of the sample was purified using the E.Z.N.A. Cycle Pure Kit (Omega Bio-Tek, Norcross, Georgia, USA). DNA was quantified using a DNA spectrophotometer (NanoDrop Technologies, Wilmington, Delaware, USA). Sequencing reactions were carried out by means of the ABI BigDye Terminator Cycle Sequencing Ready Reaction Kit version 3.1, using the ABI3730xl Genetic Analyzer (Applied Biosystems, Foster City, California, USA). Contiguous sequences were assembled in Geneious (Geneious version 9, created by Biomatters, available from (http://www.geneious.com/) and were deposited in GenBank (Table 1).

Table 1
List of myxozoan whose sequences were used for analyses and the obtained in the present study.

Parasite	GenBank accession No.	Host	Country	Reference
Ceratomyxa shasta	AF001579	Oncorhynchus mykiss	USA	Bartholomew et al. (1997)
Henneguya adiposa	EU492929	Ictalurus punctatus	USA	Griffin et al. (2009)
Henneguya bulbosus	KM000055	Ictalurus punctatus	USA	Rosser et al. (2014)
Henneguya. cerebralis	JX131380	Thymallus nigrescens	Mongolia	Batueva et al. (2013)
Henneguya. corruscans	JQ654971	Pseudoplatystoma corruscans	Brazil	Adriano et al. (2012)
Henneguya creplini	EU732597	Zingel zingel	Hungary	Eszterbauer et al. (2006)
Henneguya cuniculator	KF732840	Pseudoplatystoma corruscans	Brazil	Naldoni et al. (2014)
Henneguya cutanea	AY676460	Abramis brama	Hungary	Kallert et al. (2005)
Henneguya dogieli	KJ725078	Siniperca chuatsi	China	Unpublished
Henneguya doneci	LC011456	Carassius gibelio	China	Li et al. (2015)
Henneguya doneci	EU344898	Carassius auratus	China	Unpublished
Henneguya doneci	HM146129	Carassius gibelio	China	Ye et al. (2012)
Henneguya doori	HDU37549	Perca fluviatilis	Canada	Siddall et al. (1995)
Henneguya exilis	AF021881	Ictalurus punctatus	USA	Lin et al. (1999)
Henneguya friderici	KY315824	Leporinus friderici	Brazil	Present study
Henneguya gurlei	DQ673465	Ameiurus nebulosus	USA	Iwanowicz et al. (2008)
Henneguya ictaluri	AF195510	Ictalurus punctatus	USA	Pote et al. (2000)
Henneguya jocu	KF264964	Lutjanus jocu	Portugal	Azevedo et al. (2014)
Henneguya leporinicola	KP980550	Leporinus macrocephalus	Brazil	Capodifoglio et al. (2015)
Henneguya lobosa	EU732600	Esox lucius	Germany	Eszterbauer et al. (2006)
Henneguya maculosus	KF296344	Pseudoplatystoma corruscans	Brazil	Carriero et al. (2013)
Henneguya mississippiensis	KP404438	Ictalurus punctatus	USA	Rosser et al. (2015)
Henneguya multiplasmodialis	JQ654969	Pseudoplatystoma corruscans	Brazil	Adriano et al. (2012)
Henneguya pellis	FJ468488	Ictalurus punctatus	USA	Griffin et al. (2009)
Henneguya pellucida	KF296352	Piaractus mesopotamicus	Brazil	Carriero et al. (2013)
Henneguya piaractus	KF597016	Piaractus mesopotamicus	Brazil	Müller et al. (2013)
Henneguya pseudoplatystoma	KP981638	Pseudoplatystoma corruscans	Brazil	Milanin et al. (2015)
Henneguya pseudorhinogobii	AB447994	Rhinogobius sp.	Japan	Kageyama et al. (2009)
Henneguya psorospermica	EU732602	Esox lucius	Germany	Eszterbauer et al. (2006)
Henneguya rhinogobii	AB447992	Rhinogobius sp.	Japan	Kageyama et al. (2009)
Henneguya rotunda	KJ416130	Salminus brasiliensis	Brazil	Moreira et al. (2014a)
Henneguya salminicola	AF031411	Oncorhynchus kisutch	Canada	Hervio et al. (1997)
Henneguya sp.	JQ411297	Oncorhynchus masou masou	Japan	Yokoyama et al. (2012)
Henneguya sp.	KR704889	Cirrhinus mrigala	India	Unpublished
Henneguya sp.	EU732601	Esox lucius	Hungary	Eszterbauer et al. (2006)
Henneguya sp.	EU732599	Perca fluviatilis	Hungary	Eszterbauer et al. (2006)
Henneguya sp.	JQ690355	Carassius auratus	China	Unpublished
Henneguya sutherlandi	EF191200	Ictalurus punctatus	USA	Griffin et al. (2008)
Henneguya visibilis	KC771143	Leporinus obtusidens	Brazil	Moreira et al. (2014b)
Henneguya zikaweiensis	KR020026	Carassius auratus	China	Zhang et al. (2015)
Henneguya zschokkei	HZU13827	Prosopium williamsonii	USA	Smothers et al. (1994)
Henneguya zschokkei	AF378344	Prosopium williamsonii	Canada	Kent et al. (2001)

Alignments were subjected to maximum likelihood (ML) and Bayesian inference (BI) (rates = invgamma) analyses; additionally, Tamura & Nei (TRN) distance values were performed using Geneious. ML and BI trees were calculated under the TRN + I + G model for the sequences of the rDNA 18S, using PHYML (GUINDON & GASCUEL, 2003) and MrBayes (HUELSENBECK & RONQUIST, 2001) Geneious plug-ins for ML and BI, respectively. These models were selected using jModelTest2 (DARRIBA et al., 2012). Nucleotide frequencies were estimated from the data (A = 0.2824, C = 0.1634, G = 0.2826, T = 0.2715). Six rates of nucleotide substitution were (AC) = 1.0000, (AG) = 3.2212, (AT) = 1.0000, (CG) = 1.0000, (CT) = 6.0419, (GT) = 1.0000; proportion of invariable sites = 0.1460; gamma distribution = 0.3960 estimated with 4 rate categories. ML nodal support was estimated by 1000 nonparametric bootstrap replications. Bayesian posterior probability were determined running the Markov chains (two runs and four chains) for 4 × 10⁶ generations, discarding the initial 1/4 of sampled trees (trees sample every 4 × 10³ generations) as burn in fraction. Phylogenetic trees were rooted using Ceratonova shasta (Noble, 1950) as outgroup based upon previous Myxobolidae phylogenies (ADRIANO et al., 2009; CAPODIFOGLIO et al., 2015; NALDONI et al., 2015).

Results

Henneguya friderici cysts were found in gill filaments from ten piau specimens, i.e. 24% of the total examined. The elongated white plasmodia measured approximately 2 mm in length. The mature spores were ellipsoid in frontal view and the valves were symmetrical and convex in lateral view. The polar capsules were elongated and equal in size and occupied a little less than half of the spore body (Figure 1). Spores (N = 30) were 12.8 ± 2.1 (7.4-14.8) µm in length, 4.4 ± 0.4 (3.4-5.2) µm in width and 32.8 ± 2.6 (2.49-40) µm in total length. The bifurcated caudal processes were cylindrical, equal in size, 19.6 ± 2.2 (16.1-24.4) µm in length, and extended behind the spore. Two equal capsules were pyriform, tapering toward their anterior end and occupying nearly half of the spore, and they measured 5.1 ± 0.5 (3.7-5.9) μm in length and 1.5 ± 0.1 (1.2-1.8) μm in width (Figure 1). Table 2 provides a comparison between the data on the spore dimensions, infection sites and host of H. friderici obtained in this study and the data from the original descriptions.

Figure 1
(a) Mature spore of Henneguya friderici parasite of gill filaments of Leporinus friderici in frontal view with Nomarski interference contrast; (b) schematic of Henneguya friderici myxospore demonstrating the polar capsule, spore capsule, and caudal processes. Scale bar 10 μm.

Table 2
Comparison of the characteristics of Henneguya friderici with similar species.

Species	LS	WS	AL	TL	PCL	PCW	Host	Site	Reference
Henneguya leporinicola	7.6(5.5-8.7)	4.2 (3.6-4.9)	21.8 (12.9-32.2)	-	3.0 (2.0-3.6)	1.6 (1.2-2.0)	Leporinus macrocephalus	Gills	Martins et al. (1999)
Henneguya azevedoi	12.0(11-13)	3.2 (3-4)	39.4 (37-40)	56.4 (52-58)	6.3 (6-7)	2.1 (2-3)	Leporinus obtusidens	Gill lamellae	Barassa et al. (2012)
Henneguya caudicula	11.3 (11-12)	5.4 (5-6)	3.4 (3-4)	14.7 (14-16)	3.7 (3-4)	1.5	Leporinus lacustris	Gill filament	Eiras et al. (2008)
Henneguya friderici	10.4 (9.6-11.8)	5.7 (4.8-6.6)	23.3 (19.1-28.7)	33.8 (28.7-39.3)	4.9 (4.2-5.9)	2.1 (1.5-2.6)	Leporinus friderici	Gills	Casal et al. (2003)
Henneguya schizodon	13.1 (12-14)	3.3 (3.4)	16.3 (15-17)	28.9 (27-30)	5.4 (5-6)	1.3 (1-1.5)	Schizodon fasciatus	Kidney	Eiras et al. (2004)
Henneguya visibilis	10.8 ± 0.6	3.9 ± 0.2	18 ± 1.2	26.8 ± 1.1	4.9 ± 0.3	1.4 ± 0.1	Leporinus obtusidens	Connective tissue	Moreira et al. (2014b)
Henneguya friderici	12.8 ± 2.1 (7.4-14.8)	4.4 ± 0.4 (3.4-5.2)	19.6 ± 2.2 (16.1-24.4)	32.8 ± 2.6 (2.49-40)	5.1 ± 0.5 (3.7-5.9)	1.5 ± 0.1 (1.2-1.8)	Leporinus friderici	Gill filament	Present study

• LS: length of the spore; WS: width of the spore; AL: length of the tail; TL: total length of the spore; PCL: polar capsules length; PCW: polar capsules width.

The 18S rDNA sequencing on H. friderici spores resulted in a sequence containing 1050 bp, which was deposited in the GenBank database under accession number KY315824. This sequence was used for phylogenetic analysis. A BLAST comparison between the sequence obtained and other myxosporean sequences available in GenBank revealed that the 18S rDNA sequence of H. friderici had 92% similarity to that of Henneguya leporinicola Martins, Souza, Moraes & Moraes, 1999 (KP980550) and 89% similarity to that of H. bulbosus Rosser, Griffin, Quiniu, Khoo & Pote, 2014 (KM000055).

Similarity analysis using sequences from species that clustered closest to those produced by the present study showed that the species with greatest genetic similarity to H. friderici was H. leporinicola, with 94% similarity. The ML and BI phylogenetic tree (Figure 2) showed that H. friderici appears as a sister species of H. leporinicola in a subclade composed mainly of myxosporean parasites of Characiformes and Esociformes.

Figure 2
Maximum Likelihood from phylogenetic analysis of the sequences of 18S rDNA gene of Henneguya friderici associated with the closest species indicated by the analysis of Max Score by BLAST of the NCBI platform. First number of nodal support is from maximum likelihood bootstrap (1000 replications), the second number shows Bayesian posterior probability (for 4 × 10⁶ generations; burn-in = 4 × 10³). Sample from the present study is in bold.

Discussion

Henneguya friderici was described by Casal et al. (2003) infecting the gills, intestine, kidney and liver of L. friderici in the Amazon River, near Belém, state of Pará, Brazil. Its description was based on morphological and ultrastructural data. This was, in the past, the main method for characterization and identification of myxosporeans (MOLNÁR, 2002). However, Kent et al. (2001) and Lom & Dyková (2006) suggested that amplification of 18S rDNA is fundamental for describing new species of myxosporeans, because of the difficulties of characterizing the spores morphologically.

The present study provided 18S rDNA sequencing on H. friderici that was found infecting the gill filaments of host caught in the Mogi Guaçú River in the state of São Paulo. This enabled phylogenetic analysis on this parasite. The 18S rDNA gene is used in molecular systematics for determining relationships among myxozoans because it is highly variable between very closely related species (KENT et al., 2001). The morphometric and morphological data obtained in the present study clearly confirmed the identification of the species as H. friderici, which was originally described by Casal et al. (2003) (Table 2).

Molnár (2002) divided the formation of gill-located myxosporean plasmodia into three types: (1) lamellar; (2) filamental; and (3) gill arch. Among these, the filamental type is subdivided into four types: (1) vascular; (2) epithelial; (3) intrachondral; and (4) basifilamental. In the present study, the H. friderici plasmodia developed on the filamental epithelium of the gills and deformed the gill filaments (Figure 3).

Figure 3
Plasmodia of Henneguya friderici infecting the gill filaments of Leporinus friderici. Scale bar = 10 mm.

The prevalence of H. friderici in piau was 24%. This was close to the 30% reported by Casal et al. (2003), considering all the infected organs of L. friderici. However, in fish from the Mogi Guaçú River, infection was only observed in the gill filaments. Furthermore, these results corroborated data from other studies conducted in South America in which species of Henneguya were found at the same infection site (NALDONI et al., 2009, 2014).

These supplementary data on the morphology, 18S rDNA sequencing and phylogeny of H. friderici may facilitate accurate diagnoses and better understanding of the phylogenetic relationships of this parasite. Fiala (2006) indicated that host preference is very important and that myxosporean species could group together according to fish host species. Although host geographical origin is particularly important, tissue tropism in myxosporean evolution has also been revealed in numerous phylogenetic studies (ANDREE et al., 1999; KENT et al., 2001; ESZTERBAUER, 2004; FIALA, 2006).

Acknowledgements

To M.Sc. Júlio Cesar C. de Aguiar (CEPTA/IBAMA) for assistance in the development of the work. Letícia G. P. Vidal was supported by a Doctoral fellowship from CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico do Brasil), and José L. Luque was supported by a Researcher fellowship from CNPq.

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Publication Dates

• Publication in this collection
  16 Mar 2017
• Date of issue
  Jan-Mar 2017

History

• Received
  20 Dec 2016
• Accepted
  16 Feb 2017