Thesis
Molecular and bioinformatic analysis of the circadian clock in Phreatichthys andruzzii
Negrini, P.
Record Number:
5863
Year:
2015
University:
Università degli studi di Ferrara, Ph. D. thesis
Abstract:
Daily cycles of light and temperature imposed by the rotation of the
Earth on its axis have had a major impact on the evolution of all
living organisms. Fascinating demonstrations of this fact can be seen
in extreme environments such as caves or in the deep sea, where
some species have evolved in complete isolation from daily lightdark
cycles for millions of years, sharing a range of striking physical
characters acquired by convergent evolution such as loss of eyes
and pigmentation. One fundamental issue is to investigate whether
these “hypogean” species still retain a functional circadian clock,
which is a highly conserved self-sustaining timing system that allows
organisms to anticipate daily environmental changes and is
synchronized primarily by light. In this study, we have performed a
comparative analysis of the circadian clock between the Somalian
cavefish Phreatichthys andruzzii, which has evolved in perpetual
darkness, and the model species Danio rerio (the zebrafish) that is
evolved under natural daily light-dark cycles. It has been
demonstrated that P. andruzzii retains a food-entrainable clock that
is synchronized in response to regular feeding time, but does not
respond to light-dark cycles. Moreover, under constant conditions,
the cavefish clock oscillates with an extremely long period and also
lacks normal temperature compensation. Based on these previous
results, we started to analyze in detail one specific clock gene that is
light-induced in zebrafish, Period2, where we encountered significant
mutations in cavefish. We characterized the coding sequence and
the genomic structure of this mutated cavefish gene and we
analyzed its expression levels in comparison with zebrafish.
Subsequently, for the first time in this species we performed a
detailed characterization of clock and visual/non-visual
photoreceptor genes as part of a complete P. andruzzii genome and
transcriptome analysis. Our RNAseq analysis revealed a surprising
phenomenon in cavefish: P. andruzzii mRNA sequences present an
unusually high level of retained introns, leading to premature stop
codons being introduced into the coding sequences of many
transcripts. This mechanism may contribute to the aberrant clock
phenotype of this species as well as, from a wider perspective, to
other fascinating cavefish adaptations to life in constant darkness.
We analyzed in detail this aberrant intron splicing phenomenon in
two cavefish transcriptomes, from the brain and from a fin-derived
cell line. Finally, the creation of a first P. andruzzii genome assembly
by DNAseq analysis allowed us to map and characterize the group of
visual/non-visual opsins, the main candidate genes involved in the
circadian and non- photoreception system. We used this sequence
data in order to perform a comparative analysis of the levels of
expression of these genes between cavefish and zebrafish. Our
results suggest that the loss of photoreceptor function in cavefish
may result either from mutations affecting the coding regions of the
opsins, as documented in TMT-opsin and Opn4m2, or, alternatively,
from mutations affecting the regulation of the expression levels of
this group of photoreceptive genes.
Times Cited:
1
Relevent Species:
Related Records:
Pellegrin, J. (1931)
Les Cyprinides cavernicoles d'Afrique
Parenzan, P. (1939)Pesci del acque sotterranee della Somalia
Ercolini, A. and Berti, R. (1975)Light sensitivity experiments and morphology studies of the blind phreatic fish Phreatichthys andruzzii from Somalia
Bianchi, S. (1978)Osservazioni preliminari sulle cellule mucose di Phreatichthys andruzzii Vinciguerra, pesce freatico anoftalmo della Somalia
Messana, G. (1979)Groundwater research by the "Centro di studio par la faunistica ed ecologia tropicali" in Somalia
Delfino, G., Bianchi, S. and Ercolini, A. (1981)On the olfactory epithelium in cyprinids: A comparison between hypogean and epigean species
Andreoli, C. (1981)La flora algale presente in due particolari pozzi della Somalia meridionale
Berti, R., Thines, G. and Lefevre, B. (1982)Effets des informations chimiques provenant d'un milieu habite par des congeneres sur l'orientation topographique du poisson cavernicole Phreatichthys andruzzii Vinciguerra (Pisces, Cyprinidae)
Ercolini, A., Berti, R., Chelazzi, L. and Messana, G. (1982)Researches on the phreatobitic fishes of Somalia: Acheivements and prospects
Leveque, C. and Daget, J. (1984)Phreatichthys anduzzii Vinciguerra, 1924
Messana, G., Chelazzi, L. and Baccetti, N. (1985)Biospeleology of Somalia: Mugdile and Showli Berdi caves
Messana, G. and Chelazzi, L. (1986)The fauna of the subterranean waters of East Africa, and particularly of Somalia
Ercolini, A., Berti, R., Chelazzi, L. and Messana, G. (1987)Oxygen consumption in hypogean and epigean cyprinids (Pisces)
Berti, R. (1990)Specific chemical recognition in Phreatichthys andruzzii (Pisces, Cyprinidae)
Berti, R. and Masciarelli, L. (1993)Comparative performances of non-visual food search in the hypogean cyprinid Phreatichthys andruzzii and the epigean relative Barbus filamentosus
Sbordoni, M. C., Dematthaeis, E., Mattoccia, M., Berti, R. and Sbordoni, V. (1996)Genetic variability and differentiation of hypogean cyprinid fishes from Somalia
Frangioni, G., Berti, R. and Borgioli, G. (1997)Hepatic respiratory compensation and haematological changes in the cave cyprinid, Phreatichthys andruzzii
Messana, G. (2001)Somalia
Berti, R and Zorn, L. (2001)Locomotory responses of the cave cyprinid Phreatichthys andruzzii to chemical signals from conspecifics abd related species: new findings
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Pucci, A., Berti, R. and Simonetta, A. (2019)The skull osteology of the blind cave cyprinid Phreatichthys andruzzii Vinciguerra, 1924
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Zamani-Faradonbe, M., Keivany, Y., Dorafshan, S. and Zhang, E. (2021)Two new species of Garra (Teleostei: Cyprinidae) from western Iran
Zamani-Faradonbe M. and Keivany Y. (2021)Biodiversity and distribution of Garra species (Teleostei: Cyprinidae) in Iran
Zamani-Faradonbe, M. and Keivany, Y. (2021)Comparative osteology of two Garra species (Cypriniformes, Cyprinidae) from Hormuz and Sistan basins of Iran
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Baratti, G., Potrich, D., Lee, S.A., Morandi-Raikova, A. and Sovrano, V.A. (2022)The geometric world of fishes: A synthesis on spatial reorientation in Teleosts
Pavlova, V.V. and Krylov, V.V. (2023)Cavefishes in chronobiological research: A narrative review.