In vivo 31P-MRS of muscle bioenergetics in marine invertebrates: Future ocean limits scallops' performance

Abstract

Object: Dynamic in vivo 31 P-NMR spectroscopy in combination with Magnetic Resonance Imaging (MRI) was used to study muscle bioenergetics of boreal and Arctic scallops (Pecten maximus and Chlamys islandica) to test the hypothesis that future Ocean Warming and Acidification (OWA) will impair the performance of marine invertebrates. Materials & methods: Experiments were conducted following the recommendations for studies of muscle bioenergetics in vertebrates. Animals were long-term incubated under different environmental conditions: controls at 0°C for C. islandica and 15°C for P. maximus under ambient PCO 2 of 0.039 kPa, a warm exposure with +5°C (5°C and 20°C, respectively) under ambient PCO 2 (OW group), and a combined exposure to warmed acidified conditions (5°C and 20°C, 0.112 kPa PCO 2 , OWA group). Scallops were placed in a 4.7 T MR animal scanner and the energetic status of the adductor muscle was determined under resting conditions using in vivo 31 P-NMR spectroscopy. The surplus oxidative flux (Q max) was quantified by recording the recovery of arginine phosphate (PLA) directly after moderate swimming exercise of the scallops. Results: Measurements led to reproducible results within each experimental group. Under projected future conditions resting PLA levels (PLA rest) were reduced, indicating reduced energy reserves in warming exposed scallops per se. In comparison to vertebrate muscle tissue surplus Q max of scallop muscle was about one order of magnitude lower. This can be explained by lower mitochondrial contents and capacities in invertebrate than vertebrate muscle tissue. Warm exposed scallops showed a slower recovery rate of PLA levels (k PLA) and a reduced surplus Q max. Elevated PCO 2 did not affected PLA recovery further. Conclusion: Dynamic in vivo 31 P-NMR spectroscopy revealed constrained residual aerobic power budgets in boreal and Arctic scallops under projected ocean warming and acidification indicating that scallops are susceptible to future climate change. The observed reduction in muscular PLA rest of scallops coping with a warmer and acidified ocean may be linked to an enhanced energy demand and reduced oxygen partial pressures (PO 2) in their body fluids. Delayed recovery from moderate swimming at elevated temperature is a result of reduced PLA rest concentrations associated with a warm-induced reduction of a residual aerobic power budget. 0.32 units until 2100 [3]. Ocean warming has a direct impact on all marine ectothermal organisms, whose body temperature changes with environmental temperature. Due to thermodynamic relations, known as the Q 10 rule of van't Hoff, physiological/biochemical processes increase with increasing temperatures bearing consequences for organismal energy budget and aerobic performance [4,5]. Marine ectotherms are adapted to their environmental temperature regime implying that they are

Exploring the mechanisms behind swimming performance limits to ocean warming and acidification in the Atlantic king scallop, Pecten maximus

“…In the present study, a retrospective metabolomic analysis using 1 H-HRMAS NMR spectroscopy was conducted using tissue samples of the king scallop, Pecten maximus, from long-term incubation experiments. Our aim was to gain a better understanding of the cellular mechanisms that respond to ocean warming (OW) and acidification (OWA) in scallops, and to relate the observed changes in metabolic pathways to the reduction in swimming performance (Schalkhausser et al, 2013, Schalkhausser et al, 2014Bock et al, 2019).…”

“…In combination with a significant increase in respiration rate at 20°C, the nearly 50% reduction in P e O 2 indicated that P. maximus had surpassed its optimal temperature range and was exhibiting a progressive warming-induced mismatch between aerobic energy supply and demand (Pörtner et al, 2017). In a subsequent study on P. maximus exposed long-term to OW (20°C, 0.04 kPa PCO 2 ) and OWA (20°C, 0.112 kPa PCO 2 ; Bock et al, 2019), we investigated the availability of energy-rich phosphates, in particular PLA and inorganic phosphate (Pi) using in vivo 31 P NMR spectroscopy and calculated the mitochondrial maximum surplus oxidative flux of the phasic muscle. In both OW-and OWA-exposed scallops, PLA and maximum surplus oxidative flux of phasic muscle were reduced, which was attributed to the lower P e O 2 in the haemolymph found in OW-and OWA-exposed scallops described in Schalkhausser et al (2014).…”

“…In particular, we focused on potential pathway modifications of the intermediary metabolism of the two adductor muscle types (phasic and tonic muscle). We propose a cellular mechanism that might explain the observed limitations in whole-animal performance of P. maximus under future climate change (Schalkhausser et al, 2014;Bock et al, 2019).…”

Exploring New Frontiers in Marine Radioisotope Tracing – Adapting to New Opportunities and Challenges

“…This technique is a non-invasive, ionizing-radiation-free analytical technique that has been used to study metabolic changes in human patients in the last century (Lauterbur et al, 1980;Bell and Bhakoo, 1998). However, developments have been made in marine ecology and comparative physiology, more particularly, in the assessment of physiological (energetic) status of marine organisms, such as mollusks or fish, under changing environmental conditions (Bock et al, 2002(Bock et al, , 2019. Mainly, two in vivo techniques have been used: proton magnetic resonance spectroscopy ( 1 H-MRS) and 31 P magnetic Resonance Spectroscopy ( 31 P-MRS).…”

“…The most important are the high-energy phosphates, ATP and phosphagen (creatine phosphate or phospho-l-arginine) and their end product, inorganic phosphate, to address the energy status. Furthermore, the 31 P-NMR signal of inorganic phosphate can be used to follow acid-base regulation of cells and tissues in the same spectrum (Bock et al, 2019). Recently, in vivo 13 C-NMR spectroscopy was introduced to study metabolic pathways in marine organisms under environmental stress (Tikunov et al, 2014).…”