Impact of Exposure to Bacteria on Metabolism in the Penaeid ShrimpLitopenaeus vannamei

Abstract

We hypothesized that aggregation of bacteria and hemocytes at the gill, which occurs as part of the shrimp's antibacterial immune defenses, would impair normal respiratory function and thereby disrupt aerobic metabolism. Changes in oxygen uptake and lactate accumulation were determined in Litopenaeus vannamei, the Pacific white shrimp, following injection with either saline (control) or a strain of the gram-negative bacterium Vibrio campbellii that is pathogenic in crustaceans. The rate of oxygen uptake was determined during the first 4 h after injection and after 24 h. Injection of bacteria decreased oxygen uptake by 27% (from 11.0 to 8.2 micromol g-1 h-1) after 4 h, while saline-injected shrimp showed no change. Decreased oxygen uptake persisted 24 h after Vibrio injection. In well-aerated water, resting whole-animal lactic acid levels increased in shrimp injected with bacteria (mean=2.59 micromol lactate g-1+/-0.39 SEM, n=8) compared to saline-injected control shrimp, but this difference did not persist at 24 h. Exposure to hypercapnic hypoxia (PCO2=1.8 kPa, PO2=6.7 kPa) also resulted in significant whole-body lactic acid differences (mean=3.99 and 1.8 micromol g-1 tissue in Vibrio and saline-injected shrimp, respectively). Our results support the hypothesis that the crustacean immune response against invading bacteria impairs normal metabolic function, resulting in depression of oxygen uptake and slightly increased anaerobic metabolism.

Energy metabolism and metabolic depression during exercise inCallinectes sapidus, the Atlantic blue crab: effects of the bacterial pathogenVibrio campbellii

“…These results are similar to those of Scholnick et al (Scholnick et al, 2006) who found that the shrimp L. vannamei experienced a 27% reduction in oxygen uptake 4h after injection of V. campbellii, which declined 24h later to 40%. Reduction of aerobic metabolism is accompanied by a small, but significant, increase in anaerobic metabolism as indicated by elevated hemolymph lactate levels (Fig.3).…”

“…It is possible that these small lactate changes could be indirect results of changes in hemolymph pH (not measured) which may alter the dynamic equilibrium between lactate and pyruvate. The result is an overall metabolic depression similar to the one observed in the Pacific white shrimp (Scholnick et al, 2006).…”

“…It is perhaps surprising that aerobic metabolism in shrimp (Scholnick et al, 2006) and in blue crabs decreases profoundly following injection of a sublethal dose of bacteria. This metabolic depression is especially interesting since the gills are implicated in the immune response (Smith and Ratcliffe, 1980a;White et al, 1985;Martin et al, 2000) during which time their respiratory function declines .…”

“…Such changes in environmental conditions not only alter fundamental processes of osmoregulation, respiration, circulation, digestion and acid-base balance (for a review, see Towle and Burnett, 2006), but also immune defenses (Newman and Feng, 1982;Le Moullac and Haffner, 2000;Holman et al, 2004;Burgents et al, 2005a;Macey et al, 2008). Interestingly, new evidence suggests that mounting an immune response against bacterial infection interferes with circulation, and consequently respiration, within crustaceans Scholnick et al, 2006).…”

Shell disease in Crangon crangon (Linnaeus, 1758): The interaction of temperature and stress response

“…The hemocytes recognize and remove these foreign matters which become trapped in the gills, what might result in a decline in the respiration (Martin et al, 2000;Smith and Ratcliffe, 1980;White and Ratcliffe, 1982). Accordingly, in the Atlantic blue crab Callinectes sapidus and in the whiteleg shrimp Litopenaeus vannamei the infection with the bacterial pathogen Vibrio campbellii, impaired the respiration function and a metabolic depression of > 30% was observed Scholnick et al, 2006;Thibodeaux et al, 2009). The present and recent studies show, that a strong immune response and a protective function of the gill against invading pathogens might lead to an impairment of the respiratory function, probably due to these aggregated hemocytes that inhibit the lamellas of the gills.…”