Metabolic Cost of the Immune Response During Early Ontogeny of the Scallop Argopecten purpuratus

Abstract

The scallop Argopecten purpuratus is an important resource for Chilean and Peruvian aquaculture. Seed availability from commercial hatcheries is critical due to recurrent massive mortalities associated with bacterial infections, especially during the veliger larval stage. The immune response plays a crucial role in counteracting the effects of such infections, but being energetically costly, it potentially competes with the physiological and morphological changes that occur during early development, which are equally expensive. Consequently, in this study, energy metabolism parameters at the individual and cellular levels, under routine-basal status and after the exposure to the pathogenic strain bacteria (Vibrio splendidus VPAP18), were evaluated during early ontogeny (trochophore, D-veliger, veliger, pediveliger, and early juveniles) of A. purpuratus. The parameters measured were as follows: (1) metabolic demand, determined as oxygen consumption rate and (2) ATP supplying capacity measured by key mitochondrial enzymes activities [citrate synthase (CS), electron transport system (ETS), and ETS/CS ratio, indicative of ATP supplying efficiency], mitochondrial membrane potential (ΔΨm), and mitochondrial density (ρm) using an in vivo image analysis. Data revealed that metabolic demand/capacity varies significantly throughout early development, with trochophores being the most efficient in terms of energy supplying capacity under basal conditions. ATP supplying efficiency decreased linearly with larval development, attaining its lowest level at the pediveliger stage, and increasing markedly in early juveniles. Veliger larvae at basal conditions were inefficient in terms of energy production vs. energy demand (with low ρm, ΔΨm, enzyme activities, and ETS:CS). Post-challenged results suggest that both trochophore and D-veliger would have the necessary energy to support the immune response. However, due to an immature immune system, the immunity of these stages would rely mainly on molecules of parental origin, as suggested by previous studies. On the other hand, post-challenged veliger maintained their metabolic demand but decreased their ATP supplying capacity, whereas pediveliger increased CS activity. Overall, results suggest that veliger larvae exhibit the lowest metabolic capacity to overcome a bacterial challenge, coinciding with previous works, showing a reduced capacity to express immune-related genes. This would result in a higher susceptibility to pathogen infection, potentially explaining the higher mortality rates occurring during A. purpuratus farming.

A Diet Rich in HUFAs Enhances the Energetic and Immune Response Capacities of Larvae of the Scallop Argopecten purpuratus

“…Interestingly, aerobic support of energy metabolism was higher in the pediveliger stage (CS and ETS activities) and more efficient in the LH-fed pediveligers (ETS:CS ratios). On the other hand, as previously found [ 25 ], veliger larvae showed low aerobic energy efficiency, but this was improved in the HH-fed veligers. Indeed, during larval culture, a greater natatory capacity was observed in the HH-fed veliger larvae than in the LH-fed veliger larvae.…”

“…Additionally, during early ontogeny, massive mortalities caused by Vibrio pathogens have been observed in Argopecten purpuratus hatcheries, mainly at the veliger stage [ 41 ]. Previous findings suggest that the higher susceptibility of veliger larvae to bacterial infections would be associated with a lower metabolic capacity to support the immune response [ 14 , 25 ]. The results obtained in the present study indicate that the administration of a diet rich in highly unsaturated fatty acids (HUFAs) (an essential component in the diet of bivalve mollusks [ 33 , 63 ]) to scallop larvae increases cell membrane fluidity and energy metabolic capacity, and enhances the immune response capacity and ability to control Vibrio proliferation.…”

“…Few studies have evaluated the metabolic demand imposed by pathogenic bacterial infections in scallop larvae. In this regard, it was recently found that the A. purpuratus veliger larval stage has the highest metabolic demand and the lowest mitochondrial concentration and energy production efficiency compared with other early developmental stages [ 25 ]. This suggests that the veliger stage would have the lowest capacity to overcome pathogen infections.…”

Resistance of Argopecten purpuratus scallop larvae to vibriosis is associated with the front-loading of immune genes and enhanced antimicrobial response

“…associated with the development affected the energy metabolism of A. purpuratus larvae, that veliger larvae exhibit the lowest metabolic capacity to overcome a bacterial challenge (19). We showed in the present work that resistant scallop larvae have a higher expression of immune genes both at basal level and during early infection.…”

“…Scallop larvae were produced in the central marine culture laboratory of the Universidad Catoĺica del Norte (LCCM-UCN). To determine the Vibrio bivalvicida (VPAP30) dose to obtain 50% affected larvae, multiparental larvae were obtained from induced spawning as described in (19). Briefly, 80 mature adults (7.0 ± 0.5 cm in height) of A. purpuratus were collected from a culture in Tongoy Bay (Coquimbo, Chile).…”