Zebrafish parental progeny investment in response to cycling thermal stress and hypoxia: deposition of heat shock proteins but not cortisol

Abstract

The maternal match hypothesis predicts that maternal exposure to a stressor may help prepare offspring to cope with the same disturbance in later life. Although there is support for this hypothesis, the signals involved in non-genetic inheritance are unclear. In this study we tested how adult zebrafish exposure to diel cycles of thermal stress (27-36°C), hypoxia (20-85% dissolved oxygen), or the combined treatment affect maternal and embryonic levels of cortisol and heat shock proteins (HSPs). While parental exposure to the thermal, hypoxic, or combined treatment for 2 weeks did not affect whole-body cortisol levels, the combined exposure increased ovarian cortisol levels by 4-fold and reduced embryonic cortisol content by 60%. The combined treatment also elicited 3- and 19-fold increases in embryo transcripts involved in cortisol breakdown (11bhsd2) and export (abcb4), respectively. The thermal stress and combined exposure also elicited marked increases in ovary and embryo hsp70a (20- to 45-fold) and HSP70 (3- to 7-fold), and smaller increases in ovary and embryo hsp90aa and hsp47 (2- to 4-fold) and in embryo HSP90 and HSP47 (2- to 6-fold). In contrast, except for increases in ovary hsp90aa (2-fold) and embryo HSP90 (3-fold), the hypoxia treatment had little effect on HSP expression and transfer. Overall, while the embryonic deposition of HSPs largely paralleled the ovarian cellular stress response, the inverse relationship between ovary and embryo cortisol levels suggests barriers against cortisol deposition in response to environmental stressors. We conclude that the endocrine and cellular stress responses make stressor-specific and distinct contributions to non-genetic inheritance.

Intergenerational plasticity to cycling high temperature and hypoxia affects offspring stress responsiveness and tolerance in zebrafish

“…Embryos and larvae were processed as described in Lim and Bernier (2022) . Briefly, samples were homogenized and extracted twice with MeOH prior to C 18 column purification (100 mg octadecyl [C 18 ], 1 ml column, Agela Technologies, Tianjin, China).…”

“…The intra- and inter-assay coefficients of variation were 9.3% ( n =4) and 9.5% ( n =3), respectively. The lower detection limit of the assay is 10 pg ml −1 as determined by Lim and Bernier (2022) . According to the manufacturer, the cross-reactivity of the commercial antibody to other steroids is as follows: prednisolone 47.4%, cortisone 15.7%, 11-deoxycortisol 15.0%, prednisone 7.83%, corticosterone 4.81%, 6β-hydroxycortisol 1.37%, 17-hydroxyprogesterone 1.36% and deoxycorticosterone 0.94%.…”

“…In placental and egg-laying species, maternal stressors can increase the deposition of GCs into offspring ( Saino et al, 2005 ; Almasi et al, 2012 ; Sheriff and Love, 2013 ; Sopinka et al, 2017a ), and maternal GCs are known for their capacity to induce epigenetic modifications and shape offspring morphology, physiology and behavior ( McCormick, 1998 ; Kapoor and Matthews, 2005 ; Eriksen et al, 2011 ; Capelle et al, 2016 ; Sopinka et al, 2017b ; Best et al, 2017 ). In fish, however, it is unclear whether maternal stressors lead to an increase in offspring GC levels ( Stratholt et al, 1997 ; Sopinka et al, 2014 ; Taylor et al, 2016 ; Lim and Bernier, 2022 ; Magierecka et al, 2022 ) or whether exogenous GCs can improve offspring stressor tolerance ( Redfern et al, 2017 ; Warriner et al, 2020a , b ). In addition, fish eggs may buffer against maternally derived GCs using ATP-binding cassette efflux transporters ( Fischer et al, 2013 ; Paitz et al, 2016 ) and by converting GCs into inert forms using the catabolic enzymes 11β hydroxysteroid dehydrogenase type 2 (11β-HSD2) and 20β-HSD2 ( Alderman and Vijayan, 2012 ; Tokarz et al, 2012 ; Faught et al, 2016 ).…”

“…In addition, fish eggs may buffer against maternally derived GCs using ATP-binding cassette efflux transporters ( Fischer et al, 2013 ; Paitz et al, 2016 ) and by converting GCs into inert forms using the catabolic enzymes 11β hydroxysteroid dehydrogenase type 2 (11β-HSD2) and 20β-HSD2 ( Alderman and Vijayan, 2012 ; Tokarz et al, 2012 ; Faught et al, 2016 ). In teleosts, exposure to heat stress and/or hypoxic conditions can lead to an increase in the production of specific inducible HSPs, including HSP90α (encoded as hsp90aa ), HSP70 (encoded as hsp70a ) and HSP47 ( Krone and Sass, 1994 ; Delaney and Klesius, 2004 ; Todgham et al, 2005 ; Vinagre et al, 2012 ; Narum et al, 2013 ; Chadwick and McCormick, 2017 ; Levesque et al, 2019 ; Lim and Bernier, 2022 ). Interestingly, maternal transfer of HSPs is associated with increases in progeny thermal tolerance in both Artemia ( Norouzitallab et al, 2014 ) and Drosophila ( Lockwood et al, 2017 ).…”

“…Interestingly, maternal transfer of HSPs is associated with increases in progeny thermal tolerance in both Artemia ( Norouzitallab et al, 2014 ) and Drosophila ( Lockwood et al, 2017 ). In zebrafish, parental exposure to chronic diel cycles of heat stress and/or hypoxia can affect the embryonic deposition of GCs and inducible HSPs ( Lim and Bernier, 2022 ). Whether this dynamic parental progeny investment of GCs and HSPs is associated with intergenerational plasticity remains to be determined.…”