Reproduction Immunity Trade-Off in a Mollusk: Hemocyte Energy Metabolism Underlies Cellular and Molecular Immune Responses

Brokordt, Katherina; Defranchi, Yohana; Espósito, Ignacio; Cárcamo, Claudia B.; Schmitt, Paulina; Mercado, Luís; Fuente-Ortega, Erwin de la; Rivera‐Ingraham, Georgina A.

doi:10.3389/fphys.2019.00077

Cited by 38 publications

(15 citation statements)

References 69 publications

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“…Although several studies have described the metabolic capacities and metabolic demands in adult scallops (Wang et al, 2012 ; Brokordt et al, 2015 , 2019 ), such information is scarce for early developmental stages (larvae and juveniles). In the late 1980s and 90s, some studies described certain energetic aspects of scallop larvae, like filtration rate (energy uptake) and biochemical changes (MacDonald, 1988 ; Farías et al, 1998 ).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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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.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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“…The bivalve's affords efficient protection against different potential invaders, based on the activity of circulating immunocytes, the hemocytes, which can recognize potential pathogens and foreign particles through phagocytosis and different cytotoxic reactions, secreting soluble factors in the hemolymph fluid ( 8 – 14 ). Bivalve hemocytes, thanks to their capacity to cross epithelial barriers and the characteristics of the open circulatory system, play pleiotropic roles in other functions, such as nutrient transport, biomineralization, and reproduction ( 15 – 17 ). As more information is available on the molecular and functional traits of hemocyte function ( 18 , 19 ), understanding the potential impact of pollutant exposure on bivalve immune defense is gaining increasing attention.…”

Section: Introductionmentioning

confidence: 99%

Immunological Responses of Marine Bivalves to Contaminant Exposure: Contribution of the -Omics Approach

et al. 2021

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The increasing number of data studies on the biological impact of anthropogenic chemicals in the marine environment, together with the great development of invertebrate immunology, has identified marine bivalves as a key invertebrate group for studies on immunological responses to pollutant exposure. Available data on the effects of contaminants on bivalve immunity, evaluated with different functional and molecular endpoints, underline that individual functional parameters (cellular or humoral) and the expression of selected immune-related genes can distinctly react to different chemicals depending on the conditions of exposure. Therefore, the measurement of a suite of immune biomarkers in hemocytes and hemolymph is needed for the correct evaluation of the overall impact of contaminant exposure on the organism's immunocompetence. Recent advances in -omics technologies are revealing the complexity of the molecular players in the immune response of different bivalve species. Although different -omics represent extremely powerful tools in understanding the impact of pollutants on a key physiological function such as immune defense, the -omics approach has only been utilized in this area of investigation in the last few years. In this work, available information obtained from the application of -omics to evaluate the effects of pollutants on bivalve immunity is summarized. The data shows that the overall knowledge on this subject is still quite limited and that to understand the environmental relevance of any change in immune homeostasis induced by exposure to contaminants, a combination of both functional assays and cutting-edge technology (transcriptomics, proteomics, and metabolomics) is required. In addition, the utilization of metagenomics may explain how the complex interplay between the immune system of bivalves and its associated bacterial communities can be modulated by pollutants, and how this may in turn affect homeostatic processes of the host, host–pathogen interactions, and the increased susceptibility to disease. Integrating different approaches will contribute to knowledge on the mechanism responsible for immune dysfunction induced by pollutants in ecologically and economically relevant bivalve species and further explain their sensitivity to multiple stressors, thus resulting in health or disease.

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“…2017; Brokordt et al. 2019). In both sexes the accumulated costs of reproduction tend to lower performance later in life, increase the rate of senescence (Nussey et al.…”

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Quantifying the costs of pre- and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort

2021

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Although it is widely stated that both mating behavior and sperm traits are energetically costly for males, we currently lack empirical estimates of the relative costs to males of pre‐ versus postcopulatory investments. Such estimates require the experimental separation of the act of mating from that of ejaculation, which is a nontrivial logistical challenge. Here, we overcome this challenge using a novel morphological manipulation (gonopodium tip ablation) in the eastern mosquitofish (Gambusia holbrooki) to tease apart investment in mating effort from that in sperm replenishment following ejaculation. We quantified the relative cumulative costs of investing in mating effort and ejaculation by comparing somatic traits and reproductive performance among three types of males: ablated males that could attempt to mate but not ejaculate; unablated males that could both mate and ejaculate; and control males that had no access to females. We show that, after eight weeks, mating investment significantly reduces both body growth and immunocompetence and results in a significant decline in mating effort. In contrast, cumulative investment into sperm replenishment following ejaculation has few detectable effects that are only apparent in smaller males. These minor costs occur despite the fact that G. holbrooki has very high levels of sperm competition and multiple mating by both sexes, which is usually associated with elevated levels of sperm production. Crucially, our study is the first, to our knowledge, to experimentally compare the relative costs of pre‐ and postcopulatory investment on components of male fitness in a vertebrate.

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Reproduction Immunity Trade-Off in a Mollusk: Hemocyte Energy Metabolism Underlies Cellular and Molecular Immune Responses

Cited by 38 publications

References 69 publications

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

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

Immunological Responses of Marine Bivalves to Contaminant Exposure: Contribution of the -Omics Approach

Quantifying the costs of pre- and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort

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