Proteomic response of marine invertebrate larvae to ocean acidification and hypoxia during metamorphosis and calcification

Abstract

SUMMARYCalcifying marine invertebrates with complex life cycles are particularly at risk to climate changes as they undergo an abrupt ontogenetic shift during larval metamorphosis. Although our understanding of the larval response to climate changes is rapidly advancing, the proteome plasticity involved in a compensatory response to climate change is still unknown. In this study, we investigated the proteomic response of metamorphosing larvae of the tubeworm Hydroides elegans, challenged with two climate change stressors, ocean acidification (OA; pH 7.6) and hypoxia (HYP; 2.8 mg O 2 l −1 ), and with both combined. Using a twodimensional gel electrophoresis (2-DE)-based approach coupled with mass spectrometry, we found that climate change stressors did not affect metamorphosis except under OA, but altered the larval proteome and phosphorylation status. Metabolism and various stress and calcification-related proteins were downregulated in response to OA. In OA and HYP combined, HYP restored the expression of the calcification-related proteins to the control levels. We speculate that mild HYP stress could compensate for the negative effects of OA. This study also discusses the potential functions of selected proteins that might play important roles in larval acclimation and adaption to climate change.Supplementary material available online at http://jeb.biologists.org/lookup/suppl

Effect of temperature rise and ocean acidification on growth of calcifying tubeworm shells (<i>Spirorbis spirorbis</i>): an in situ benthocosm approach

“…Most studies have focused on the tropical species Hydroides elegans (Lane et al, 2013;Chan et al, 2012Chan et al, , 2013Mukherjee et al, 2013;Li et al, 2014). The results indicated reduced growth, increased porosity and reduced mechanical strength of the worm tubes, as well as increased mortality of larvae at lowered pH (< 7.9).…”

Changing mineralogical properties of shells may help minimize the impact of hypoxia-induced metabolic depression on calcification

“…These mechanical properties are mainly determined by the quantity of matrix proteins occluded in the shell, which can exceptionally augment the mechanical strength Addadi et al, 2006;Marin et al, 2008). Our findings, therefore, imply that similar amount of metabolic energy can still be allocated to the 180 production of matrix proteins under hypoxia (Mukherjee et al, 2013), so that the mechanical strength can be maintained. When energy budget becomes limited, this energy allocation strategy (i.e.…”

“…Yet, some calcifying organisms have been shown to maintain calcification under hypoxia (Mukherjee et al, 2013;Nardelli et al, 2014;Keppel et al, 2016). It is favourable because shell growth is vital for not only continuing somatic growth, but also offering physical protection, especially under life-threatening conditions (e.g.…”

“…Since hypoxia can be persistent, or even permanent, as observed in many coastal and marine waters 225 worldwide (Helly and Levin, 2004;Diaz and Rosenberg, 2008), the survival of some calcifying organisms under persistent hypoxia suggests that they may have evolved the capacity to accommodate its impacts on energy metabolism and hence maintain calcification (Mukherjee et al, 2013;Frieder et al ,2014;Nardelli et al, 2014;Keppel et al, 2016). …”

Calcification and inducible defence response of a calcifying organism could be maintained under hypoxia through phenotypic plasticity

“…However, few previous studies showed that some calcifying organisms are able to maintain calcification under hypoxia (Mukherjee et al, 2013;Frieder et al, 2014;Keppel et al, 2016), and even anoxia (Nardelli et al, 2014). These unexpected results suggest potential mechanisms which can compensate for the reduced metabolic energy under hypoxia in order to sustain calcification.…”