DISEASES OF AQUATIC ORGANISMSDis Aquat Org

INTRODUCTION

The class Myxosporea Bütschli, 1881 of the phylumMyxozoa Grassé, 1970 contains about 60 genera (Lom& Dyková 2006); however, this number was recentlyincreased by the addition of 4 new genera. Among themyxosporeans, the genus Henneguya Thélohan, 1892,which contains at least 204 species, is the second mostspeciose genus (Lom & Dyková 1992, 2006). There arenumerous detailed descriptions of this genus found

from fishes from all continents, of which 40 have beendescribed from the Brazilian fauna. However, most ofthese descriptions are based on light microscopy anddiagrammatic drawings of the mature spores (Cunha &Fonseca 1918, Nemeczek 1926, Pinto 1928a,b, Gui-marães & Bergamin 1933, 1934, Jakowska & Nigrelli1953, Walliker 1969, Cordeiro et al. 1983/1984, Kent &Hoffman 1984, Gioia et al. 1986, Martins & Souza 1997,Eiras 2002, Barassa et al. 2003a,b, Eiras et al. 2004a,b,2008, 2009, Martins & Onaka 2006, Abdallah et al.

© Inter-Research 2011 · www.int-res.com*Email: azevedoc@icbas.up.pt

Henneguya torpedo sp. nov. (Myxozoa), a parasitefrom the nervous system of the Amazonian teleost Brachyhypopomus pinnicaudatus (Hypopomidae)

Carlos Azevedo1, 2,*, Graça Casal1, 3, Patrícia Matos4, Ângela Alves1, Edilson Matos5

1Department of Cell Biology, Institute of Biomedical Sciences (ICBAS/UP and CIIMAR/UP), University of Porto, Lg. A. Salazar no. 2, 4099-003 Porto, Portugal

2Zoology Department, College of Science, King Saud University, Riyadh, Saudi Arabia3Departamento de Ciências, Instituto Superior de Ciências da Saúde - Norte, CESPU, Gandra, Portugal

4Laboratory of Aquatic Animals, Federal University of Pará, Belém, Pará, Brazil5Carlos Azevedo Research Laboratory, Federal Rural University of the Amazonia, Belém, Pará, Brazil

ABSTRACT: A new species of Myxosporea, Henneguya torpedo sp. nov., is described from the brainand spinal cord of the Amazonian teleostean fish Brachyhypopomus pinnicaudatus collected from thePeixe Boi River, State of Pará, Brazil. The spores were surrounded by a thick hyaline sheath that ishomogeneous and electron translucent and consists of 2 layers of different densities. The total sporelength is 48.62 ± 0.51 µm (mean ± SE), the ellipsoidal spore body length is 28.53 ± 0.36 µm, the bodywidth is 7.25 ± 0.31 µm and the body thickness is 3.06 ± 0.26 µm. Each of the 2 equal-sized valves pre-sented a tapering tail (19.64 ± 0.44 µm in length). The 2 equal-sized thin and smooth valves sur-rounded 2 equal-sized and elongated ellipsoidal polar capsules (6.41 ± 0.26 × 1.84 ± 0.19 µm) thatcontained 5 to 6 (rarely 7) polar filament coils. The binucleated sporoplasm contained numerousspherical sporoplasmosomes (~260 × ~280 nm) with a laterally eccentric-dense structure containing ahalf-crescent section. The sporoplasmosomes are surrounded by a hyaline homogenous sheath.Based on the data obtained by light and electron microscopy and on the host specificity, the sporesdiffered from the previously described Henneguya spp., mainly in the presence of a sheath surround-ing the spores, the spore shape and size and the number and arrangement of the polar filament coils.Therefore, from this description we propose the establishment of a new species, which we havenamed Henneguya torpedo sp. nov.

KEY WORDS: Nervous system · Teleost · Brachyhypopomus pinnicaudatus · Myxosporean · Spores ·Henneguya torpedo sp. nov. · Ultrastructure

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Vol. 93: 235–242, 2011doi: 10.3354/dao02292

Published February 22

Dis Aquat Org 93: 235–242, 2011

2007). Recently, several ultrastructural studies on thestages of the developmental life-cycle and on maturespores supported the descriptions of several Hen-neguya spp. (Casal et al. 1997, 2003, Azevedo & Matos2002, 2003, Vita et al. 2003, Adriano et al. 2005,Azevedo et al. 2008, 2009, 2010, Naldoni et al. 2009). Inthe present paper, we present light microscope andtransmission electron microscope (TEM) data of sporesof a new myxosporidian, named H. torpedo sp. nov.,which parasitizes the nervous system of a Brazilian fishfrom the Amazonian region.

MATERIALS AND METHODS

Thirty specimens of the freshwater fish Brachyhy-popomus pinnicaudatus (Teleostei, Hypopomidae)(Brazilian common name ‘ituí tuanga’) were collectedfrom Peixe Boi River, a tributary of the lower AmazonRiver (01° 11’ S, 47° 18’ W), near the city of Peixe Boi,State of Pará, in northeastern Brazil. Sampling was car-ried out during January and February 2010. The fishwere transported live to the laboratory and maintainedin an aquarium at 28 to 30°C, where their behaviourwas observed for 3 to 5 d. They were later anaes-thetized with MS-222 (Sandoz Laboratories), killedand dissected. Small fragments of infected tissues werethen excised and examined under a light microscopewith Nomarski differential interference contrast (DIC)optics for observation and measurement of the spores.For ultrastructural studies, small fragments of infectedtissues were fixed in 5% glutaraldehyde in 0.2 Msodium cacodylate buffer (pH 7.2) for 20 to 24 h,washed overnight in the same buffer and postfixed in2% OsO4 buffered in the same solution for 4 h, all at4°C. After dehydration in an ascending graded ethanolseries and propylene oxide, samples were embeddedin Epon epoxy resin. Semithin sections were stainedwith methylene blue-Azur II stain. Ultrathin sectionswere double-stained with aqueous uranyl acetate andlead citrate and observed in a JEOL 100CXII TEMoperated at 60 kV.

RESULTS

The only parasitized organs of the fish were thebrain and the spinal cord in which some tailed sporesappeared randomly distributed throughout the ner-vous tissue. The parasitized fish showed some abnor-mal and abrupt movements, sometimes projectingthemselves against the wall of the aquarium. Observedunder DIC, the spores were easily identified as belong-ing to the genus Henneguya Thélohan, 1892, owing totheir ellipsoidal morphology with 2 equal-sized smooth

valves, each one bearing a tapering caudal projectionforming a tail (Figs. 1 & 2). Of the 30 fish, 10 (33.3%)were parasitized.

Henneguya torpedo sp. nov.

Based on the morphological (see Figs. 1 & 2) and ultra-structural aspects (see Figs. 3 to 8 & 12) of the valvedmulticellular spores and on the polar nature of the cap-sules, which contained a coiled polar filament, togetherwith the host specificity, we described this parasite asHenneguya torpedo sp. nov., a new species with thefollowing description:

Phylum: Myxozoa Grassé, 1970Class: Myxosporea Bütschli, 1881Order: Bivalvulida Shulman, 1959Family: Myxobolidae Thélohan, 1892Genus: Henneguya Thélohan, 1892

Life history stages

Comparative measurements (in µm) of spores with asurrounding sheath from different species of Hen-neguya including H. torpedo sp. nov. are described inTable 1. Only spores (Fig. 1) were observed randomlydistributed in the nervous tissue of the brain and spinalcord of H. torpedo sp. nov. (Fig. 2).

Description

The spores were surrounded by a hyaline homoge-neous sheath adherent to the spore body wall (Figs. 3to 8) and tails (Figs. 9 to 12) that conforms to the shapeof the spores. This sheath was composed of an exter-nal, moderate light, electron-dense layer and an inter-nal layer that is less electron dense, both of more orless similar thickness: 0.92 µm; range: 0.80 to 0.98 µm)(Figs. 3 to 7 & 9 to 12). Including the thickness of thesurrounding sheath, the total length (mean ± SE) of themature spores was 48.62 ± 0.51 µm (range: 48.3 to 48.9µm; n = 25). The spore bodies were ellipsoidal with alength of 28.53 ± 0.36 µm (range: 28.3 to 30.1 µm; n =25), width of 7.25 ± 0.31 µm (range: 7.0 to 7.5 µm; n =15), thickness of 3.06 ± 0.26 µm (range: 2.9 to 3.1 µm; n= 25), and tail length of 19.64 ± 0.44 µm (range: 19.2 to19.9 µm; n = 15) (Figs. 1, 3 to 7 & 9 to12). The 2 equal-sized polar capsules were 6.41 ± 0.26 µm (range: 6.3 to6.6 µm; n = 20) long and 1.84 ± 0.19 µm (range: 1.7 to1.9 µm; n = 20) wide (Figs. 1 & 3 to 5). The number ofpolar filament coils ranged from 5 to 6, rarely 7 (Figs. 3& 4). The spore wall was thin and smooth comprising 2equal-sized valves (Figs. 3 to 7), each one with a taper-

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Azevedo et al.: Ultrastructural studies of Henneguya torpedo sp. nov.

ing caudal projection forming the tail (Figs. 1 & 9 to12). The binucleated sporoplasm was located in theposterior pole of the spore and contained 2 nucleilocated side by side and several sporoplasmosomes(Figs. 6 & 7). The sporoplasmosomes were globular(260 ± 32 × 280 ± 49 nm, n = 25) formed by an electron-dense matrix and contained an eccentric dense struc-ture with a half-crescent section (Figs. 6 to 8) and weresurrounded by a homogenous lighter sheath ~25 nm inthickness (Figs. 8 & 13). The following is a summary ofthe findings.

Type host: The spores were observed only in thebrain and spinal cord tissues of the freshwater fishBrachyhypopomus pinnicaudatus (Teleostei, Hypopo-midae).

Type locality: Peixe Boi River (Lower Amazonregion) (01° 11’ S, 47° 18’ W), near the city of Peixe Boi,State of Pará, Brazil.

Prevalence: Ten out of 30 (33.3%); 7 out of 18(38.8%) for females and 3 out of 12 (25%) for males.

Type specimens: A slide with semithin sections con-taining the hapantotypes of the spores randomly dis-tributed in the nervous tissues was deposited in theInternational Protozoan Type Slide Collection at theSmithsonian Institution, Washington, DC 20560, USA(USNM no. 2055216).

Etymology: The specific epithet derives from thespore morphology that seems to have a torpedo form.

Histopathology: The nervous tissue located in theneighbouring zone, in which the spores were located,presents a more evident ultrastructural disorganiza-tion, mainly in specimens with a higher number ofspores (Figs. 9 to 12). Some parasitized fish specimensexhibited disturbed movements, sometime projectingthemselves against the glass walls of the aquarium.

DISCUSSION

All the observed characteristics confirmed the mor-phological similarities of the spores of the differentspecies of the genus Henneguya previously described(Lom & Dyková 2006) and in particular their similarityto Henneguya spp. reported in the nervous system ofteleosts (Kent & Hoffman 1984, Azevedo et al. 2008)(see Table 1). Although the spore of H. torpedo sp. nov.resembles that of H. theca, the first Henneguya spp.described within the nervous system of fish (Kent &Hoffman 1984), there are some morphological differ-ences between these spores that are important inclearly distinguishing these 2 species.

The main criteria for comparison among the differentHenneguya spp. are the presence or absence of a sur-rounding sheath, spore shape, spore length and width,polar capsule (PC) shapes, size measurements and the

237

Tab

le 1

. H

enn

egu

yasp

p.

Com

par

ativ

e m

easu

rem

ents

(in

µm

mea

n w

ith

ran

ge

in p

aren

thes

es)

of s

por

es w

ith

a s

urr

oun

din

g s

hea

th f

rom

dif

fere

nt

spec

ies

of H

enn

egu

yath

at p

aras

itiz

e th

e n

ervo

us

syst

em o

f fis

hes

. TL

: tot

al le

ng

th; S

BL

: sp

ore

bod

y le

ng

th; S

BW

: sp

ore

bod

y w

idth

; SB

T: s

por

e b

ody

thic

kn

ess;

TaL

: tai

l len

gth

; PC

L: p

olar

cap

sule

le

ng

th; P

CW

: pol

ar c

apsu

le w

idth

; nP

FC

: no.

of

pol

ar f

ilam

ent

coil

s; (

–): n

o d

ata

Hen

neg

uya

sp

p.

Hos

t sp

ecie

s an

dT

LS

BL

SB

WS

BT

TaL

PC

LP

CW

nP

FC

Sou

rce

org

ans/

tiss

ues

H. t

hec

aE

igem

ann

ia v

ires

cen

s b

rain

48.0

24.8

3.5

–23

.211

.11.

4–

Ken

t &

Hof

fman

(19

84)

(40.

6–

52.6

)(3

.0–

4.1)

(20.

3–2

4.2)

(9.8

–12.

5)(1

.0–1

.6)

H. r

ond

oni

Gym

nor

ham

ph

ich

thys

ron

don

i17

.77.

03.

62.

510

.72.

50.

856

–7

Aze

ved

o et

al.

(20

08)

per

iph

eral

ner

vou

s sy

stem

(16.

9–1

8.1)

(6.8

–7.

3)(3

.0–

3.9)

(2.2

–2.8

)(1

0.3

–11.

0)(2

.2–2

.7)

(0.7

9–

0.88

)

H. t

orp

edo

sp. n

ov.

Bra

chyh

ypop

omu

s p

inn

icau

dat

us

48.6

228

.53

7.25

3.06

19.6

46.

411.

846

–7

Pre

sen

t st

ud

yb

rain

/sp

inal

cor

d(4

8.3

–48

.9)

(28.

3–

30.1

)(7

.0–

7.5)

(2.9

–3.

1)(1

9.2

–19.

9)(6

.3–

6.6)

(1.7

–1.9

)

Dis Aquat Org 93: 235–242, 2011238

Azevedo et al.: Ultrastructural studies of Henneguya torpedo sp. nov. 239

Figs. 9 to 12. Henneguya torpedo sp. nov. Transmission electron micrographs of the spore of the myxosporean parasite from thenervous system of the Amazonian teleostean fish Brachyhypopomus pinnicaudatus (scale bars in µm). Fig. 9. Longitudinal sectionof the transitional region of the spore body (S) and the initial portion of the 2 tails (T) showing the surrounding homogenoussheath (*). Fig. 10. Transverse section of the tails (T) and the sheath (*) in contact with the disorganized nervous tissue (H). Fig. 11. Transverse sections of 4 tails (T) and a spore (S) located among the host nervous tissue, all surrounded by the homo-

geneous sheath (*). Fig. 12. Longitudinal sections of the tails (T) and the surrounding sheath (*)

Figs. 1 to 8. Henneguya torpedo sp. nov. Light and transmission electron micrographs of the myxosporean parasite found in thenervous system of the Amazonian teleostean fish Brachyhypopomus pinnicaudatus (scale bars in µm). Fig. 1. Living spores ob-served by means of differential interference contrast microscopy. Fig. 2. Semithin section of several spores (S) sectioned at differ-ent levels located within the nervous system (H). Fig. 3. Ultrathin longitudinal section of a spore body showing the homogenoussheath (*) composed of 2 layers, the valves (V), the 2 polar capsules (PC), the polar filaments and their transverse sections (arrow-heads) and the sporoplasm (Sp) with sporoplasmosomes. Fig. 4. Ultrathin section of a polar capsule (PC) showing some details ofthe apical region (arrow), the capsule wall (W) and different polar filament sections (arrowheads). Fig. 5. Transverse section of aspore at polar capsules (PC) level, showing the valves (V) and their sutures lines (arrowheads) surrounded externally by thesheath (*) formed by 2 layers, all located within the nervous system (H). Fig. 6. Longitudinal section of the basal portion of thespore body showing the external sheath (*), the valves (V), the nuclei (N) and sporoplasmosomes (Sps). The parasite is in contactwith the host nervous tissue (H). Fig. 7. Ultrathin transverse section of the spore body sectioned at the nucleus level (N) where nu-merous sporoplasmosomes (Sps) are present. In this section the sheath (*), the valves (V) and the host tissue (H) can be observed.Fig. 8. Ultrastructural detail of sporoplasmosomes (Sps) with an eccentric dense structure with a half-crescent section, both

formed by a dense matrix and a surrounding homogenous sheath (arrowheads)

Dis Aquat Org 93: 235–242, 2011

internal arrangements of the polar filaments (i.e. num-ber of coils and their position in relation to the PC axis)(Lom & Dyková 2006). However, because the greatmajority of Henneguya spp. have been described fromlight microscope observations and diagrammaticdrawings of the spores, it is difficult to establish pointsof similarity with which to compare several Henne-guya spp.

The homogeneous sheath that surrounds the sporeshas been described in only 6 other species of the genusHenneguya: H. theca (Kent & Hoffman 1984), H. ama-zonica (Rocha et al. 1992), H. adherens (Azevedo &Matos 1995), H. malabarica (Azevedo & Matos 1996),H. testicularis (Azevedo et al. 1997) and H. rondoni(Azevedo et al. 2008); in contrast to H. torpedo sp. nov.,however, these species — with the exception ofH. theca and H. rondoni — were found to parasitize or-gans or tissues other than the nervous system of fishes.

When comparing Henneguya torpedo sp. nov. withother species parasitizing the nervous system of fish,the presence of a sheath surrounding the spore seemsto be an important characteristic that should be consid-ered. While all surfaces of the spores of H. torpedo sp.

nov. had a complex and thick sheath composed of 2layers of different electron densities, the H. thecaspore had a thinner sheath surrounding the spore(Kent & Hoffman 1984), whereas the H. rondoni sporehad a thin homogeneous hyaline sheath, which sur-rounded only the tails (Azevedo et al. 2008).

The total spore lengths of Henneguya torpedo andH. theca were similar; however, the spore body lengthand spore width of the former were larger, while thetails of the latter were longer.

The total spore size and the tail and spore body sizeswere all smaller in Henneguya rondoni compared withthose in H. torpedo sp. nov. Also, the dimensions of thepolar capsules were larger in H. torpedo spores.H. rondoni spores were only detected in cysts locatedin the peripheral nervous fibres of the lateral line of thefish’s body (Azevedo et al. 2008), while the H. torpedospores were observed in the brain and spinal cordtissues.

Unfortunately, since the previous descriptions ofHenneguya theca spores were not made from TEMobservations, we found it difficult, using our results, tocompare characteristics such as the number of polar fil-ament coils, the organization of the sporoplasmosomesand the type of sheath.

On the other hand, comparison of our observationswith all the other Henneguya spp. observations listedby Eiras (2002), including the recently described newspecies, demonstrates that most of the characteristicsare rather different.

We present a semi-schematic drawing of a spore ofHenneguya torpedo sp. nov. (Fig. 14) showing specificcharacteristics, such as spore shape and dimensions,the 2 equal-sized polar capsules and an evident thickhyaline sheath surrounding the spores. Based on themorphological and ultrastructural differences des-cribed, the host specificity, and the presence of ahomogenous and hyaline sheath surrounding thespore, we are able to justify the establishment of thisnew species, which we have named Henneguya tor-

240

Fig. 14. Henneguya torpedo sp. nov. Semi-schematic drawing of a valvar view of the spore of the myxosporean parasite from thenervous system of the Brazilian freshwater teleost Brachyhypopomus pinnicaudatus obtained from light microscopy and ultra-structural data, showing species-specific characteristics such as a thick sheath surrounding all surfaces of the spore, the sporeshape and size, 2 equal-sized polar capsules, binucleated sporoplasm and 2 equal-sized tails. Some measurements (total length,

body length, polar capsule length and tail length) were obtained from ultrathin serial sections

Fig. 13. Henneguya torpedo sp. nov. Schematic drawing of thesporoplasmosome measuring ~280 × 260 nm at its greatestbreadth and surrounded by a homogenous sheath (~25 nm thick)

Azevedo et al.: Ultrastructural studies of Henneguya torpedo sp. nov.

pedo sp. nov. This study shows that the proposed newspecies, H. torpedo sp. nov., is the first to be recordedin the brain and spinal cord of Brazilian teleost fishes.

Acknowledgements. This study was partially supported bythe Eng. A. Almeida Foundation, Porto, Portugal, CNPq andCAPES (Brazil). The excellent technical assistance of J. Car-valheiro is gratefully acknowledged. The various aspects ofthis work complied with the current laws of the countries inwhich they were carried out.

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Editorial responsibility: David Marcogliese,Montreal, Quebec, Canada

Submitted: July 22, 2010; Accepted: September 28, 2010Proofs received from author(s): January 28, 2011