Efeitos genéticos, endócrinos e transgeracionais do estresse térmico sobre as células germinativas em truta arco-íris (Oncorhynchus mykiss)
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2020-05-31
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Universidade Estadual Paulista (Unesp)
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Em peixes, exposições a altas temperaturas podem afetar a proliferação, diferenciação ou mesmo a sobrevivência das células germinativas, comprometendo a fertilidade e, portanto, a capacidade reprodutiva das espécies. Há também evidências de alterações epigenéticas que podem eventualmente ser transmitidas às próximas gerações, tendo implicações sobre a sobrevivência e capacidade adaptativa aos ambientes sujeitos às constantes mudanças. Este trabalho buscou elucidar os mecanismos regulatórios (molecular e endócrino) e transgeracionais envolvidos na manutenção e diferenciação das células germinativas em truta arco-íris (Oncorhynchus mykiss) submetidas a estresse térmico prolongado. Para tanto, foram avaliados inicialmente os efeitos da exposição a alta temperatura durante a fase juvenil (parr) nas gônadas de adultos, comparando os parâmetros reprodutivos e qualidade dos gametas. Em seguida, estes foram utilizados em cruzamentos, visando comparar o desempenho das respectivas progênies (WT) com as do grupo controle (CT) quando submetidas ao estresse térmico. Finalmente, foram realizados experimentos in vitro com testículos de juvenis destas progênies buscando correlacionar a tolerância térmica com a susceptibilidade ao cortisol, o principal hormônio do estresse. Os resultados da primeira etapa demonstraram que o estresse térmico afetou nitidamente mais os machos que as fêmeas, sendo os efeitos deletérios detectados no desenvolvimento testicular, na fecundidade, na motilidade e morfologia espermática, e também no desenvolvimento embrionário. Surpreendentemente, apesar de tais impactos negativos, a progênie derivada dos machos estressados submetidas às mesmas condições estressantes que os pais apresentaram sobrevida e crescimento superiores, demonstrando que o estresse térmico nos parentais pode conferir termotolerância na prole após uma única geração. Desempenho similar foi observado usando progênies de machos de três anos de idade, sugerindo alterações constitutivas nas espermatogônias-tronco. A análise in vitro demonstrou que os testículos da progênie WT apresentaram menor susceptibilidade ao cortisol comparado com o grupo CT, sugerindo que o grupo WT possui maior capacidade de neutralizar os efeitos do estresse. As demais análises de transcrição gênica, que foram interrompidas em função da pandemia do COVID-19, poderão elucidar os aspectos moleculares envolvidos na tolerância à temperatura alta. Em conclusão, este estudo demonstra que o estresse térmico durante as fases iniciais pode induzir efeitos permanentes em aspectos reprodutivos essenciais durante a fase adulta e ainda modular a capacidade adaptativa da respectiva progênie, quando submetidas às mesmas condições que os parentais. Estas descobertas agregam uma nova abrangência acerca dos impactos das mudanças climáticas em peixes, mas ao mesmo tempo indicam a existência de mecanismos que permitem os animais superarem as alterações no ambiente, desde que a sobrevivência das gerações seguintes, mesmo que limitada, seja garantida. No caso das espécies de interesse comercial, a estratégia utilizada neste estudo pode contribuir para o desenvolvimento de linhagens com maior resiliência a fatores ambientais.
In fish, exposure to high temperatures can affect the proliferation, differentiation or even survival of germ cells, compromising fertility and the reproductive capacity of the species. There is also evidence of epigenetic changes that may eventually be transmitted to the next generations, determining the survival and adaptive capacity of animals submitted to constant changing environments. The aim of this work was to elucidate the regulatory (molecular and endocrine) mechanisms and transgenerational effects involved in the maintenance and differentiation of germ cells in rainbow trout (Oncorhynchus mykiss) subjected to thermal stress. For this purpose, the effects of exposure to high temperatures during parr stages were initially evaluated on adult gonads, by comparing reproductive parameters and gamete quality. Then, these gametes were used in crosses, in order to compare the performance of respective offspring (WT) in relation to control group (CT), upon exposure to thermal stress. Finally, in vitro experiments with juvenile testis from the same progenies were performed with the purpose to find a relationship between thermal tolerance and the susceptibility to cortisol, the main stress hormone. The results of the first section demonstrated that the thermal stress clearly affected more the males than females, wherein deleterious effects were detected on testis development, fecundity, sperm motility and morphology, and also on embryo development. Surprisingly, in spite of those negative impacts, the progeny derived from stressed males subjected to the similar stressful conditions as their parents showed superior survival and growth, which demonstrate that thermal stress in parental fish can somehow confer thermotolerance in the offspring after a single generation. A similar performance was observed using progenies derived from three-year-old males, which points to constitutive alterations in spermatogonial stem cells. In vitro analysis revealed a lower susceptibility to cortisol in WT in relation to CT group, which suggests that the first may have a higher capacity to buffer the effects of stress. The remaining gene transcription analysis - which were interrupted due to COVID-19 pandemic - may elucidate the molecular aspects involved in the acquisition of high temperature tolerance. In conclusion, this study demonstrates that thermal stress during juvenile stages can induce permanent effects on essential reproductive features at adult stage and also modulate the adaptive capacity of the respective progeny, when they are exposed to similar conditions as those of their parents. These findings add a new dimension on the impacts of climate change in fish, but at the same time indicate the existence of mechanisms that allow animals to overcome the changing environment, given that the survival of next generations, even restricted, are ensured. As for commercially important species, the approach used in this study can contribute to the development of strains displaying higher resilience to particular environmental conditions.
In fish, exposure to high temperatures can affect the proliferation, differentiation or even survival of germ cells, compromising fertility and the reproductive capacity of the species. There is also evidence of epigenetic changes that may eventually be transmitted to the next generations, determining the survival and adaptive capacity of animals submitted to constant changing environments. The aim of this work was to elucidate the regulatory (molecular and endocrine) mechanisms and transgenerational effects involved in the maintenance and differentiation of germ cells in rainbow trout (Oncorhynchus mykiss) subjected to thermal stress. For this purpose, the effects of exposure to high temperatures during parr stages were initially evaluated on adult gonads, by comparing reproductive parameters and gamete quality. Then, these gametes were used in crosses, in order to compare the performance of respective offspring (WT) in relation to control group (CT), upon exposure to thermal stress. Finally, in vitro experiments with juvenile testis from the same progenies were performed with the purpose to find a relationship between thermal tolerance and the susceptibility to cortisol, the main stress hormone. The results of the first section demonstrated that the thermal stress clearly affected more the males than females, wherein deleterious effects were detected on testis development, fecundity, sperm motility and morphology, and also on embryo development. Surprisingly, in spite of those negative impacts, the progeny derived from stressed males subjected to the similar stressful conditions as their parents showed superior survival and growth, which demonstrate that thermal stress in parental fish can somehow confer thermotolerance in the offspring after a single generation. A similar performance was observed using progenies derived from three-year-old males, which points to constitutive alterations in spermatogonial stem cells. In vitro analysis revealed a lower susceptibility to cortisol in WT in relation to CT group, which suggests that the first may have a higher capacity to buffer the effects of stress. The remaining gene transcription analysis - which were interrupted due to COVID-19 pandemic - may elucidate the molecular aspects involved in the acquisition of high temperature tolerance. In conclusion, this study demonstrates that thermal stress during juvenile stages can induce permanent effects on essential reproductive features at adult stage and also modulate the adaptive capacity of the respective progeny, when they are exposed to similar conditions as those of their parents. These findings add a new dimension on the impacts of climate change in fish, but at the same time indicate the existence of mechanisms that allow animals to overcome the changing environment, given that the survival of next generations, even restricted, are ensured. As for commercially important species, the approach used in this study can contribute to the development of strains displaying higher resilience to particular environmental conditions.
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Peixes, Truta, Gametogênese, Células germinativas, Espermatogônias, Temperatura, Estresse Térmico