Morphology, seasonality and phylogenetic relationshipsof Ceratomyxa husseini n. sp. from the gall-bladderof Cephalopholis hemistiktos (Ruppell) (Perciformes:Serranidae) in the Arabian Gulf off Saudi Arabia

Abdel-Azeem S. Abdel-Baki • Lamjed Mansour •

Hussain A. Al-Qahtani • Suliman Y. Al Omar •

Saleh Al-Quraishy

Received: 12 December 2014 / Accepted: 18 February 2015

� Springer Science+Business Media Dordrecht 2015

Abstract During a survey of myxosporean parasites

of marine fishes from the Arabian Gulf in Saudi

Arabia, spores of Ceratomyxa husseini n. sp. were

found in the gall-bladders of 50 out of 148 specimens

(33.8%) of the yellowfin hind Cephalopholis hemistik-

tos (Ruppell) (Perciformes: Serranidae). The rates of

infection showed a seasonal fluctuation, with the

highest prevalence in winter and the lowest in autumn.

The mature spores appeared arched in frontal view

with rounded valve ends and a slightly discriminated

curved suture line and measured 8–9 9 14–18

(9 9 16) lm. The two polar capsules were spherical

and equal in size, 4–5 (4.5) lm in diameter. The polar

filament showed four turns obliquely to the longitu-

dinal axis of the capsules and the sporoplasm filled

half of the entire spore cavity. Partial sequences of the

small subunit rRNA gene of C. husseini n. sp. showed

percentage of identity with other species of Cerato-

myxa ranging between 79.8 and 92.7%. The morpho-

metric and molecular data, in association, confirmed

that the present new species differs from all other

Ceratomyxa spp. reported to date.

Introduction

Members of genus Ceratomyxa Thelohan, 1892 are

myxozoan parasites of marine teleosts (Gunter et al.,

2009). The genus is one of the largest within the

phylum Myxozoa Grasse, 1970, with about 200

described species that comprise nearly 8% of the

known myxosporeans (Lom & Dykova, 2006; Gunter

et al., 2009; Azevedo et al., 2013). Cephalopholis

Bloch & Schneider is the most common genus of the

family Serranidae Innamura & Yabe in the aquarium

trade and some species of this genus feature colourful

bodies (Abied et al., 2014). The genus comprises 22

species (FAO, 2002). Of these, Cephalopholis

hemistiktos (Ruppell) is one of the most abundant

species that appears to have a disjunctive distribution,

being known with certainty only from the northern

part of the Red Sea, and from the Arabian Gulf to the

coast of the Pakistan Gulf (Randall, 1995).

To date, nine species of Ceratomyxa have been

described from fish members of the family Serranidae.

Ceratomyxa angusta Meglitsch, 1960 from Hypoplec-

trodes semicinctum (Valenciennes) and C. gemmaphora

A.-A. S. Abdel-Baki (&) � L. Mansour �H. A. Al-Qahtani � S. Y. Al Omar � S. Al-Quraishy

Zoology Department, College of Science, King Saud

University, P.O. Box 2455, Riyadh 11451, Saudi Arabia

e-mail: azema1@yahoo.com

A.-A. S. Abdel-Baki

Zoology Department, Faculty of Science, Beni-Suef

University, Beni-Suef, Egypt

L. Mansour

Unite de Recherche de Biologie integrative et Ecologie

evolutive et Fonctionnelle des Milieux Aquatiques,

Departement de Biologie, Faculte des Sciences de Tunis,

Universite De Tunis El Manar, Tunis, Tunisia

123

Syst Parasitol (2015) 91:91–99

DOI 10.1007/s11230-015-9554-3

Meglitsch, 1960 from Caesioperca lepidoptera (For-

ster) were both described in the Pacific Ocean off New

Zealand (Meglitsch, 1960). Ceratomyxa brayi Gunter &

Adlard, 2009 and C. whippsi Gunter & Adlard, 2009

from Cephalopholis boenak (Bloch), C. cutmorei Gun-

ter & Adlard, 2009 from Epinephelus fasciatus (For-

sskal), C. gleesoni Gunter & Adlard, 2009 from

Plectropomus leopardus (Lacepede), C. hooperi Gunter

& Adlard, 2009 and C. nolani Gunter & Adlard, 2009

from Epinephelus quoyanus (Valenciennes) and

C. yokoyamai Gunter & Adlard, 2009 from Epinephelus

maculatus (Bloch) were all described in fishes from the

Great Barrier Reef, Australia (see Gunter & Adlard,

2009). Regarding Saudi Arabia, so far two species of

Ceratomyxa have been described from fishes in the

Arabian Gulf: C. hamour Mansour, Al-Qahtani, Al-

Quraishy & Abdel-Baki, 2015 and C. arabica Al-

Qahtani, Mansour, Al-Quraishy & Abdel-Baki, 2015

(see Al-Qahtani et al., 2015; Mansour et al., 2015).

In this paper we describe a new species of

Ceratomyxa parasitising the gall-bladder of Cephalo-

pholis hemistiktos (Ruppell) (Perciformes: Ser-

ranidae) collected from the Arabian Gulf off Saudi

Arabia. The description is based on morphometric and

rDNA sequence data. Data on the seasonal variation in

prevalence are also provided for this new species.

Materials and methods

Samples of C. hemistiktos were collected during the

period from February 2013 to February 2014. A total

148 fish was sampled from the Arabian Gulf off

Dammam (26�3302000N, 50�002500E), Saudi Arabia.

The fish were examined for myxosporean infections,

with gall-bladder infections being verified by micro-

scopic examination of bile, collected by puncturing

the gall-bladder with a finely-pointed glass pipette.

Fresh spores were observed and photographed using

an Olympus BX51 microscope fitted with an Olympus

DP71 Camera. Measurements were calibrated using a

micrometre and were based on 45 fresh spores.

Description and measurements of spores follow the

guidelines of Lom & Arthur (1989); the latter are

presented as the range followed by the mean in

parentheses. Infected gall-bladders were preserved in

85% ethanol for DNA analysis.

DNA was extracted from three single isolated gall-

bladders filled with mature spores and preserved in

85% ethanol. Spores were pelleted, ethanol was

removed and the pellet was washed three times with

a saline buffer. Extraction was performed using the

QIAGEN DNeasy kit (QIAGEN Inc., Valencia,

California, USA) according to the instructions of the

manufacturer.

For molecular characterisation, a partial fragment

of the small subunit (SSU) rRNA gene was amplified

using the primers MyxospecF (50-TTC TGC CGT

ATC AAC TWG TTG-30) (Fiala, 2006) and 18R (50-CTA CGG AAA CCT TGT TAC G-30) (Whipps et al.,

2003). PCR reactions were processed as reported by

Mansour et al. (2015). Fragments from three different

PCR products were sequenced by Macrogen Inc.

(Seoul, South Korea), using the PCR primers.

A consensus sequence of 1,529 bp was deposited in

GenBank. The deposited sequence was used to query

similar sequences through a standard nucleotide-nu-

cleotide BLAST (blastn) (Altschul et al., 1997). The

most similar SSU rDNA sequences of 26 species of the

genus Ceratomyxa were retrieved from GenBank

(Table 1). Myxobolus ampullicapsulatus Zhao, Sun,

Kent, Deng & Whipps, 2008 was used as an outgroup.

Sequences were aligned with ClustalX 2.1.0.12, apply-

ing the default parameters (Larkin et al., 2007). The

maximum likelihood and neighbour joining trees were

constructed using MEGA software v.5 package (Tamura

et al., 2011). The maximum likelihood tree was obtained

using the Kimura 2-parameter model (Kimura, 1980).

The best-fit substitution model (K80?G?I) was selected

on the basis of the lowest score of Bayesian Information

Criterion (BIC) calculated with the MEGA package.

Bootstrap support was based on 1,000 replicates.

Fisher’s exact test was performed to compare

prevalences using Quantitative Parasitology web

software Version 1.0.9 (Reiczigel et al., 2014). The

results were considered significant at p B 0.05.

Ceratomyxa husseini n. sp.

Type-host: Cephalopholis hemistiktos (Ruppell) (Per-

ciformes: Serranidae), yellowfin hind.

Type-locality: Arabian Gulf off Dammam

(26�3302000N, 50�002500E), Saudi Arabia.

92 Syst Parasitol (2015) 91:91–99

123

Type-material: Syntype spores in 80% ethanol are

deposited in the parasitological collection of the

Hungarian Natural History Museum under the inven-

tory number HNHM-70619.

Site of infection: The infection was detected as large

clusters of free floating spores in the bile solution.

Vegetative stages were not observed.

Prevalence: 33.8% (overall prevalence; in 50 out of

148 specimens examined).

Representative sequence: One SSU rDNA sequence

(1,529 bp) is deposited in GenBank under accession

number KP262017.

Etymology: The specific name is given in honour of the

late Professor Dr. Hussein Ser-Elkhatam Hussein,

Zoology Department, College of Science, King Saud

University, Saudi Arabia.

Table 1 GenBank accession numbers for Ceratomyxa spp. used in the phylogenetic analysis and percentage of identity (P) between

these species and Ceratomyxa husseini n. sp.

Species Accession

numbers

P (%) Reference

C. husseini n. sp. KP262017 – Present study

C. brayi Gunter & Adlard, 2009 EU729697 92.7 Gunter & Adlard (2009)

C. hooperi Gunter & Adlard, 2009 EU729692 91.4 Gunter & Adlard (2009)

C. puntazzi Alama-Bermejo, Raga & Holzer, 2011 JF820290 91.0 Alama-Bermejo et al. (2011)

C. barnesi Gunter, Whipps & Adlard, 2009 FJ204245 90.9 Gunter et al. (2009)

C. cardinalis Heiniger & Adlard, 2013 JX971436 90.5 Heiniger & Adlard (2013)

C. arabica Al-Qahtani, Mansour, Al-Quraishy & Abdel-Baki, 2014 KJ631533 90.4 Al-Qahtani et al. (2014)

C. whippsi Gunter & Adlard, 2009 EU729694 90.0 Gunter & Adlard (2009)

C. labracis Sitja-Bobadilla & Alvarez-Pellitero, 1993 AF411472 89.6 Palenzuela et al. (2002)

C. auerbachi Kabata, 1962 EU616734 89.5 Køie et al. (2008)

C. atkinsoni Gunter, Whipps & Adlard, 2009 FJ204244 88.8 Gunter et al. (2009)

C. bartholomewae Gunter, Burger & Adlard, 2010 GU136391 88.6 Gunter et al. (2010)

C. ostorhinchi Heiniger & Adlard, 2013 JX971425 88.5 Heiniger & Adlard (2013)

C. cyanosomae Heiniger & Adlard, 2013 JX971424 88.4 Heiniger & Adlard (2013)

C. nolani Gunter & Adlard, 2009 EU729698 88.2 Gunter & Adlard (2009)

C. rueppellii Heiniger & Adlard, 2013 JX971423 87.5 Heiniger & Adlard (2013)

C. thalassomae Heiniger, Gunter & Adlard, 2008 EU045332 86.8 Heiniger et al. (2008)

C. gleesoni Gunter & Adlard, 2009 EU729693 86.6 Gunter & Adlard (2009)

C. robertsthomsoni Gunter, Whipps & Adlard, 2009 FJ204253 86.1 Gunter et al. (2009)

C. buri Yokoyama & Fukuda, 2001 AB530264 85.2 Yokoyama et al. (2010)

C. sewelli Gunter & Adlard, 2008 EU440362 84.8 Gunter & Adlard (2008)

C. hamour Mansour, Al-Qahtani, Al-Quraishy & Abdel-Baki, 2014 KJ200360 84.7 Mansour et al. (2014)

C. lunula Gunter & Adlard, 2008 EU440378 84.3 Gunter & Adlard (2008)

C. falcatus Gunter & Adlard, 2008 EU440361 83.7 Gunter & Adlard (2008)

C. anko Freeman, Yokoyama & Ogawa, 2008 DQ301510 80.0 Freeman et al. (2008)

C. pantherini Gunter, Burger & Adlard, 2010 GU136393 79.8 Gunter et al. (2010)

Myxobolus ampullicapsulatus Zhao, Sun, Kent, Deng & Whipps,

2008 (outgroup)

KC425224 66.1 Zhao et al. (2013)

Syst Parasitol (2015) 91:91–99 93

123

Description (Figs. 1–6)

Mature spores Mature spores arched in frontal view

with rounded valve ends, 8–9 (9 ± 0.2) 9 14–18

(16 ± 0.3); suture line curved and slightly discriminat-

ed (Figs. 1–6); anterior spore margin convex, posterior

margin concave. Polar capsules 2, essentially spherical

and equal in size, 4–5 (4.5 ± 0.1) in diameter, with

capsular opening near sutural line at anterior pole of

spore. Polar filament turned four times obliquely to

longitudinal axis of capsules. Sporoplasm binucleated,

filling half of entire spore cavity (Figs. 1–6).

Figs. 1–5 Fresh spores of Ceratomyxa husseini n. sp. from the gall-bladder of Cephalopholis hemistiktos. Scale-bars: 10 lm

94 Syst Parasitol (2015) 91:91–99

123

Seasonal variation in prevalence

The overall prevalence was 33.8% and infection

occurred throughout the year, with the highest preva-

lence in winter 54% (20/37) followed by spring 37.8%

(14/37), summer 27% (10/37) and autumn 16.2%

(6/37). The data showed highly significant seasonal

pattern of prevalence (p = 0.0047) essentially due to

the significant differences between winter and summer

(p = 0.0323) and autumn (p = 0.0013) samples; no

other significant differences in prevalence were found

(all p [ 0.05).

Phylogenetic analysis

The newly obtained 1,529 bp SSU rDNA sequence

had no identical one deposited in GenBank. The

highest percentage of identity was observed with

sequences for C. brayi (92.7%) and C. hooperi

(91.4%), ceratomyxan species reported to infect the

serranid fishes Cephalopholis boenak, and Epinephe-

lus quoyanus, respectively, from the Great Barrier

Reef, Australia (Gunter & Adlard, 2009). The per-

centage of identity with other Ceratomyxa spp. varied

between 79.8 and 91.4% (Table 1). Phylogenetic trees

inferred from SSU rDNA sequences using ML and NJ

methods had similar topologies. Figure 7 shows the

ML tree obtained from the alignment of the new and

26 other sequences for Ceratomyxa spp. available in

the GenBank. Ceratomyxa husseini n. sp. species

clustered in a clade containing C. hooperi, C. brayi

and C. whippsi with consistent bootstrap values.

Discussion

A review of the available literature revealed that seven

species fall within the morphometric range of the

present species (Table 2). These similar species differ,

however, from the present species in several ways.

Ceratomyxa beloneae Lubat, Radujkovic, Marques &

Bouix, 1989, C. brayi Gunter & Adlard, 2009, C. gibba

Meglitsch, 1960, C. nolani Gunter & Adlard, 2009 and

C. recta Meglitsch, 1960 all have shorter spores and

smaller polar capsules (see Eiras, 2006; Gunter &

Adlard, 2009). In addition, C. gibba has unequal

valves and unequal polar capsules whereas C. brayi

has thicker spores. Ceratomyxa recurvata Davis, 1917

differs from the new species in having intensely

curved spores with unequal valves (see Eiras, 2006).

Finally, C. sprenti Moser, Kent & Dennis, 1989 has

stubby, shorter and thicker spores with smaller polar

capsules (see Eiras, 2006).

In addition to the morphometric data, molecular

tools confirmed that the present new species differs

from all Ceratomyxa spp. reported to date. Thus, the

lowest percentage of divergence (7.3%) was observed

between the new species and the morphometrically

comparable species C. brayi. This percentage of

divergence is large enough to confirm the distinction

between the two species. Furthermore, recently, our

team reported two new species of Ceratomyxa, C.

arabica Al-Qahtani, Mansour, Al-Quraishy & Abdel-

Baki, 2015 and C. hamour Mansour, Al-Qahtani, Al-

Quraishy & Abdel-Baki, 2015 (see Al-Qahtani et al.,

2015; Mansour et al., 2015) which, like the species

reported here, were described from fishes in the

Arabian Gulf off Saudi Arabia. These two species

infected the twobar sea bream Acanthopagrus bifas-

ciatus (Forsskal) (Sparidae) and the orange-spotted

grouper Epinephelus coioides (Hamilton) (Ser-

ranidae), respectively. In addition to the morpho-

logical differences, the percentages of identity were

low (90.4% with C. arabica and 84.7% with C.

hamour). This combination of data support our

consideration of the form infecting C. hemistiktos

described here as new.

During the present study, infections of Cephalo-

pholis hemistiktos with C. husseini n. sp. were detected

throughout the year and showed a seasonal fluctuation,

Fig. 6 Schematic drawing of a mature spore of Ceratomyxa

husseini n. sp. Scale-bar: 10 lm

Syst Parasitol (2015) 91:91–99 95

123

with the highest prevalence in winter and the lowest in

autumn. The seasonality could be explained by the

parasite development, in that the myxospore formation

is probably synchronised with the development of

actinospores in an as yet unknown intermediate host

(Yemmen et al., 2013). Also, some authors have

suggested that the seasonal patterns of myxosporean

infection may be due to environmental factors (Foott

& Hedrick, 1987; Yokoyama & Fukuda, 2001). Water

temperature is one such environmental factor that has

been suggested to have a considerable effect on the

development of myxozoans in fish and invertebrate

hosts, leading to modifications in prevalence (Kent

et al., 2001; Yemmen et al., 2013). The study by

Haaparanta et al. (1994) associated low prevalence of

infection during the summer with increased water

temperatures and immunity of the fish after the stress

of spring spawning subsided. Additionally, Yokoyama

& Fukuda (2001) suggested that the seasonal variation

in prevalence of Ceratomyxa spp. could be explained

by the variable condition of bile secretion at each

sampling period.

Fig. 7 Phylogenetic tree for Ceratomyxa spp. based on maximum likelihood analysis (Ln = -7461.98) using the SSU rDNA dataset

showing the position of C. husseini n. sp. C. nolani Bootstrap values based on 1,000 replicates are indicated at the nodes. Only bootstrap

values above 70 are shown. Myxobolus ampullicapsulatus was used as an outgroup

96 Syst Parasitol (2015) 91:91–99

123

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Syst Parasitol (2015) 91:91–99 97

123

Acknowledgement We extend our appreciation to the Dean

of Scientific Research, King Saud University, for funding the

work through the research group project number RGP-004.

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