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Tissue specific structural variations of mitochondria of fish ectoparasite Argulus bengalensis Ramakrishna, 1951 (Crustacea: Branchiura): Functional implications - PubMed

Tissue specific structural variations of mitochondria of fish ectoparasite Argulus bengalensis Ramakrishna, 1951 (Crustacea: Branchiura): Functional implications

Anirban Banerjee et al. J Adv Res. 2014 May.

Abstract

We studied the fine structure of some classical and six variant mitochondria from different tissues viz. proboscis gland, spinal gland, ovary, testis, and muscle of a fish ectoparasite, Argulus bengalensis. In the proboscis gland and spinal gland, mitochondria are protected within vesicle to preserve their structure and activity from exposure to glandular synthesis for its parasitic mode of feeding. In the oocytes, mitochondria are larger and cylindrical in appearance. Oocyte mitochondria are highly dynamic and exhibit frequent fission and fusion. Those are clustered in the cytoplasm of previtellogenic oocytes which prepare for different synthetic activities for successful reproductive investment. In contrast, mitochondrial abundance is less in the male gametic lineage. The spermatocytes and the nurse cells in the testis have an unusual type of mitochondria, nebenkern which is formed by the fusions of number of mitochondria. A completely different type of mitochondrion is discovered in the flagellum of the spermatozoa. It is provided with fifteen numbers of singlet microtubules at its outer periphery which is a salient feature of the flagellum of this Branchiuran genus. This unique mitochondrion uses the microtubule tract for its movement to distribute energy efficiently along the axoneme. Such mitochondrion and microtubular association provide evidence in favor of phylogenetic relationship between Argulus and pentastomid Raillietiella. In striated muscle of thoracic appendages, mitochondria maintain tight junctions with the endoplasmic reticulum and remain in close apposition of the myofibrils which helps in Ca(2+) uptake for stimulating continuous muscular activity required for ventilation of respiratory structures of the parasites.

Keywords: Argulus bengalensis; Fish ectoparasite; Functional correlation; Mitochondrial diversity.

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Figures

Fig. 1
Fig. 1

Photomicrograph of Argulus bengalensis and transmission electron micrograph of mitochondrial forms in the glandular cells associated with feeding apparatus. (a) Ventral view of a male showing the anatomical position of proboscis gland (pg) indicated by paired side boxes and spinal gland (sg) indicated by lower median box. (b) Transmission electron micrograph of proboscis gland: mitochondria (mt) are arranged within a separate hub (h) surrounding the nucleus (n). The cristae of these mitochondria are of condensed type. The mitochondria distributed outside the hub are provided with orthodox cristae. Bar, 2 μm. (c) Transmission electron micrograph of spinal gland: mitochondria (mt) are enclosed within vesicles (v) in the cytoplasm. Bar, 1 μm.

Fig. 2
Fig. 2

Light and electron microscopy of mitochondria in the oocytes of Argulus bengalensis. (a) Light micrograph after mitochondria specific vital staining with Janus green B showing distribution pattern of mitochondria within the cytoplasm of an early previtellogenic oocyte (o); mitochondrial clouds (indicated by boxes) are differentiated beside the nucleus (n). Bar, 18 μm. (b) Transmission electron micrograph of an early previtellogenic oocyte showing similar mitochondria rich zone around the nucleus (n). Numerous small vesicles or granulofibrillar material (GFM) are distributed within this mitochondria rich zone. (c) Ultrastructure of mitochondrion of an early previtellogenic oocyte exhibiting its tubular cristae with dilated terminal. The mitochondrion exhibits a loose association with an ER. Numerous small but dense granules (g) are observed within the inner matrix. Bar, 0.34 μm. (d) A magnified view (2×) of the association of mitochondria with ER – showing tethers (t) and ribosomes (r) in the upper pannel, and the lower panel is the schematic diagram of the same. Bar, 0.2 μm.

Fig. 3
Fig. 3

Transmission electron micrograph of oocyte mitochondria at dynamic state in Argulus bengalensis. The upper left panel exhibits out pocketing, an indication of fission of mitochondria. The upper right panel exhibits mitochondrial fusion indicated by diffused membrane (arrow head) between mitochondria. The lower left panel shows two mitochondria immediately after completion of fission. Bar, 0.54 μm. The graphic in the lower right panel represents number of mitochondria (Mt) in four previtellogenic oocytes (O1, O2, O3, and O4); mitochondria undergoing fusion or fission are counted as a single unit. Mean of five readings with ±standard error is presented in the graphics.

Fig. 4
Fig. 4

Transmission electron microscopy of mitochondria in the testicular cells of Argulus bengalensis. (a) Nebenkern (N) in the nurse cell (Nc). Nurse cell is present in between the primary (Ps) and secondary spermatocytes (Ss). The nebenkern (N) is positioned at the base of the cytoplasmic projection (P). Small classical mitochondria (mt) are also randomly distributed beside the nucleus (n) of the nurse cell. (b) Primary spermatocyte also exhibits a large nebenkern (N) beside its nucleus (n) and small classical mitochondria (mt) are randomly distributed around the nebenkern. Bar, 1 μm. (c) Magnified view (4 ×) of the nebenkern showing its stacked zigzag cristae. Bar, 0.2 μm. (d) Highly magnified view (17×) of the nebenkern showing cristae with overlapping at regular interval. The right corner panel is a schematic diagram shows the arrangement of cristae and variation in cristae diameter. Bar, 54 nm.

Fig. 5
Fig. 5

Transmission electron micrograph of mitochondria in the sperm flagellum of Argulus bengalensis. (a) Mitochondrial (mt) alignment surrounding the axoneme (Ax). (b) Three vesicular filamentous mitochondria immediately adjacent to the axoneme with clearly distinguishable outer membrane (om), inner membrane (im) and transverse cristae (tc). Cristae are uniting at the central meeting point (mp) to compartmentalize the inner matrix. Bar, 74 nm. (c) An unusual association of mitochondrion with numerous microtubules (am). The transverse cristae (tc) are originated from the inner membrane and extending up to the inner membrane of the opposite side. Twenty F1 particles are arranged near the base of each cristae. Bar, 74 nm. The bottom left panel is a magnified (6×) view showing the microtubular association with the outer membrane (om) by motor protein (mp). Bar, 13 nm. The bottom right panel is a diagrammatic representation of the microfilament. The microfilament is a complete circle of twelve protofilament (pf). It remains attached with the outer mitochondrial membrane (om) with a motor protein (mp).

Fig. 6
Fig. 6

Transmission electron microscopy of mitochondria in the striated muscle. (a) Mitochondrion (mt) in association with sarcoplasmic reticulum (Sr) showing attached putative ER vesicle (ERv). A narrow space is present in between the outer membrane (om) and the inner membrane (im). (b) Higher magnified (5×) view of the ER vesicle (ERv) showing tethers (t) and associated ribosome (r). Right panel is a schematic diagram showing molecular bridges that regulate the close contacts between ER and mitochondria. Bar, 43 nm. (c) Tight association of the ER with outer membrane (om) of a mitochondrion. Bar, 70 nm. Right panel is a magnified view of the same.

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References

    1. Palade G.E. An electron microscope study of the mitochondrial structure. J Histochem Cytochem. 1953;1:188. - PubMed
    1. Bereiter-Hahn J., Voth M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc Res Techniq. 1994;27:198–219. - PubMed
    1. Chan D.C. Mitochondrial fusion and fission in mammals. Annu Rev Cell Dev Biol. 2006;22:79–99. - PubMed
    1. Frey T.G., Mannella C.A. The internal structure of mitochondria. Trends Biochem Sci. 2000;25:319–324. - PubMed
    1. Attardi G., Schatz G. Biogenesis of mitochondria. Annu Rev Cell Biol. 1988;4:289–333. - PubMed

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