Label-free microscopy and stress responses reveal the functional organization of Pseudodiaptomus marinus copepod myofibrils

Ibrahim, Ali; Hage, Charles Henri; Souissi, Anissa; Leray, Aymeric; Héliot, Laurent; Souissi, Sami; Vandenbunder, Bernard

doi:10.1016/j.jsb.2015.06.004

Cited by 8 publications

(8 citation statements)

References 56 publications

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“…The second unusual feature is the extreme scarcity of mitochondrial profiles, with practically none being present between the supermyofibrils and only a few at the fibers' periphery. This segregation has also been demonstrated by in situ images of mitochondria detected by flavin autofluorescence (Ibrahim et al, ).…”

Section: Resultssupporting

confidence: 53%

Functionally Driven Modulation of Sarcomeric Structure and Membrane Systems in the Fast Muscles of a Copepod (Gaussia princeps)

Glaser

Iyer

Gilly

et al. 2018

The Anatomical Record

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Muscles of the mesopelagic copepod Gaussia princeps (Arthropoda, Crustacea, Calanoida) are responsible for repetitive movements of feeding and swimming appendages that are too fast to be followed by eye. This article provides a comparative functional and ultrastructural description of five muscles that have different contraction speeds and are located within different anatomical sites. All are very fast, as indicated by a thick:thin filament ratio of 3:1 and sarcomere lengths that vary between 1 and 3 μm. Measured lengths of thin and thick filaments indicate classification of the muscles into three distinct groups (short, medium, and long) and predict a difference in speed of up to threefold between fibers with the shortest and longest sarcomeres. Indeed, the kicking movement of the posterior legs (with the shortest sarcomere length) is approximately threefold faster than the simultaneous back‐folding of the antennae (with the longest length). Thus, a specific relationship between speed of movement and sarcomere length is established, and we can use the latter to predict the former. Regulatory systems of contraction (sarcoplasmic reticulum [SR] and transverse [T] tubules) match the different contractile properties, varying in frequency of distribution and overall content in parallel to sarcomere variations. All muscles from appendages and body musculature show a unique disposition of contractile material, SR, and T tubules found only in copepod muscles; muscle filaments are grouped in large supermyofibrils that are riddled with frequent cylindrical shafts containing SR and T tubules. This arrangement insures a high spatial frequency of regulatory components. Anat Rec, 301:2164–2176, 2018. © 2018 Wiley Periodicals, Inc.

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Section: Resultssupporting

confidence: 53%

Functionally Driven Modulation of Sarcomeric Structure and Membrane Systems in the Fast Muscles of a Copepod (Gaussia princeps)

Glaser

Iyer

Gilly

et al. 2018

The Anatomical Record

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“…At the low temperature of 8.0°C P. marinus responded kinematically to the electrical stimuli by performing jumps through the sequential movement of the thoracic limbs (Gemmell & Buskey, ). The experiments by Ibrahim et al () evidenced thermal and haline shock in P. marinus , with most individuals becoming comatose in 75 min upon instantaneous reduction in T from 18.0°C to 4.0°C, and only in 1 min when also salinity was abruptly changed from 30.0 to 0.0 psu. These authors suggested that acute haline and thermal changes might induce myofibril stress in P. marinus , while the results presented in this study reveal a strong adaptability of this calanoid when temperature and saline variations occur over time spans of hours to days.…”

Section: Discussionmentioning

confidence: 96%

Section: Discussionmentioning

confidence: 99%

“…Ibrahim et al (2015) and Ibrahim et al (2016) investigated the effect of thermal and haline stress on the behavior, muscle fiber and cuticle structure of P. marinus. They reported that instantaneous drastic changes in temperature and salinity induced coma and myofibril stress (Ibrahim et al, 2015), with damages to muscular tissues (Ibrahim et al, 2016). Chen, Sheng, Lin, Gao, and Lv (2006) studied the survival of the congeneric Pseudodiaptomus annandalei after salinity change, highlighting an optimum at S = 15 psu.…”

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confidence: 99%

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Response to salinity and temperature changes in the alien Asian copepod Pseudodiaptomus marinus introduced in the Black Sea

et al. 2019

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The salinity tolerance and the effect of temperature were studied on the behavior and motor activity of the nonindigenous Indo‐Pacific calanoid copepod Pseudodiaptomus marinus, first found in Sevastopol Bay (Black Sea) in autumn 2016. According to the index of median lethal salinity (LS50), the salinity tolerance range of adult P. marinus collected at 18.0 psu in November 2016 and subsequently reared in the laboratory amounted to 5.0–44.0 psu, independently of the acclimation regime. Females of P. marinus collected in December 2016 at 12.0°C became torpid at 8.0°C, a value typical of winter–spring Black Sea coastal areas. An increase in temperature from 8.0°C to 27.0°C led to an increase in the beat frequency of mouth appendages, swimming speed, and time spent cruising. However, at the same high temperature, the mean cruising speed in the feeding‐current feeder P. marinus was 2‐fold lower than that of the native, similarly sized cruise feeder Pseudocalanus elongatus. On the contrary, mouthpart beat frequency while cruising was 2‐fold higher reaching 80 Hz, due to the creation of feeding currents in P. marinus. The results of our experiments confirm the euryhaline character of P. marinus, and point to an apparent ability to survive cold temperatures in a torpid state. This suggests the possibility of entering an overwintering stage to survive the adverse cold winter–spring environmental conditions of the Black Sea, similarly to the recent thermophilic Indo‐Pacific invader Oithona davisae which established a successful population in the same area.

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“…It was also observed that the distribution of stripes in cardiomyocytes is modified after a sudden uniaxial static strain, with weakly stained regions giving the appearance of gaps within a periodic pattern [47]. As previously demonstrated for Xenopus laevis [44], nonlinear optical microscopes as above could provide more precise information on sarcomere structure changes along Pseudodiaptomus marinus copepod myofibers subjected to thermal and haline stresses [48]. Besides its advantage, nonlinear optical microscopy is freely and easily available only to a relatively small number of scientists, while CLSM are present and accessible in most institutes today.…”

Section: Discussionmentioning

confidence: 92%

Myofibril Changes in the Copepod Pseudodiaptomus marinus Exposed to Haline and Thermal Stresses

Ibrahim¹,

Souissi²,

Leray³

et al. 2016

PLoS ONE

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Copepods are small crustaceans capable to survive in various aquatic environments. Their responses to changes in different external factors such as salinity and temperature can be observed at different integration levels from copepod genes to copepod communities. Until now, no thorough observation of the temperature or salinity effect stresses on copepods has been done by optical microscopy. In this study, we used autofluorescence to visualize these effects on the morphology of the calanoid copepod Pseudodiaptomus marinus maintained during several generations in the laboratory at favorable and stable conditions of salinity (30 psu) and temperature (18°C). Four different stress experiments were conducted: at a sharp decrease in temperature (18 to 4°C), a moderate decrease in salinity (from 30 to 15 psu), a major decrease in salinity (from 30 to 0 psu), and finally a combined stress with a decrease in both temperature and salinity (from 18°C and 30 psu to 4°C and 0 psu). After these stresses, images acquired by confocal laser scanning microscopy (CLSM) revealed changes in copepod cuticle and muscle structure. Low salinity and/or temperature stresses affected both the detection of fluorescence emitted by muscle sarcomeres and the distance between them. In the remaining paper we will use the term sarcomeres to describe the elements located within sarcomeres and emitted autofluorescence signals. Quantitative study showed an increase in the average distance between two consecutive sarcomeres from 2.06 +/- 0.11 μm to 2.44 +/- 0.42 μm and 2.88 +/- 0.45μm after the exposure to major haline stress (18°C, 0 psu) and the combined stress (4°C, 0 psu), respectively. These stresses also caused cuticle cracks which often occurred at the same location, suggesting the cuticle as a sensitive area for osmoregulation. Our results suggest the use of cuticular and muscle autofluorescence as new biomarkers of stress detectable in formalin-preserved P. marinus individuals. Our label-free method can be easily applied to a large number of other copepod species or invertebrates with striated musculature.

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Label-free microscopy and stress responses reveal the functional organization of Pseudodiaptomus marinus copepod myofibrils

Cited by 8 publications

References 56 publications

Functionally Driven Modulation of Sarcomeric Structure and Membrane Systems in the Fast Muscles of a Copepod (Gaussia princeps)

Functionally Driven Modulation of Sarcomeric Structure and Membrane Systems in the Fast Muscles of a Copepod (Gaussia princeps)

Response to salinity and temperature changes in the alien Asian copepod Pseudodiaptomus marinus introduced in the Black Sea

Myofibril Changes in the Copepod Pseudodiaptomus marinus Exposed to Haline and Thermal Stresses

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