Physiological and metabolic responses to hypoxia in invertebrates

Grieshaber, Manfred K.; Hardewig, I.; Kreutzer, Ulrike; Pörtner, Hans‐Otto

doi:10.1007/bfb0030909

Cited by 301 publications

(292 citation statements)

References 261 publications

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“…At these extremely high concentrations, Cr is at the solubility limit and may be trapped in the extracellular matrix and at the whiskered cell wall of yeast cells, thus escaping washing procedures. 4 In fact, the very low concentration of PCr observed in these yeast cells rather suggests that Cr is separated from the cytosolic CK and is therefore mainly (if not entirely) extracellular. Remnant PCr may have been produced by CK that is possibly liberated from a few damaged cells.…”

Section: Discussionmentioning

confidence: 91%

Functional Expression of Phosphagen Kinase Systems Confers Resistance to Transient Stresses in Saccharomyces cerevisiae by Buffering the ATP Pool

Canonaco¹,

Schlattner²,

Pruett³

et al. 2002

Journal of Biological Chemistry

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Phosphagen kinase systems provide different advantages to tissues with high and fluctuating energy demands, in particular an efficient energy buffering system. In this study we show for the first time functional expression of two phosphagen kinase systems in Saccharomyces cerevisiae, which does not normally contain such systems. First, to establish the creatine kinase system, in addition to overexpressing creatine kinase isoenzymes, we had to install the biosynthesis pathway of creatine by co-overexpression of L-arginine:glycine amidinotransferase and guanidinoacetate methyltransferase. Although we could achieve considerable creatine kinase activity, together with more than 3 mM intracellular creatine, this was not sufficient to confer an obvious advantage to the yeast under the specific stress conditions examined here. Second, using arginine kinase, we successfully installed an intracellular phosphagen pool of about 5 mM phosphoarginine. Such arginine kinase-expressing yeast showed improved resistance under two stress challenges that drain cellular energy, which were transient pH reduction and starvation. Although transient starvation led to 50% reduced intracellular ATP concentrations in wild-type yeast, arginine kinase overexpression stabilized the ATP pool at the pre-stress level. Thus, our results demonstrate that temporal energy buffering is an intrinsic property of phosphagen kinases that can be transferred to phylogenetically very distant organisms.The availability of biochemical energy, with ATP as the primary energy currency, is fundamental to most cellular processes. Although ATP and its congeners are involved in literally hundreds of biochemical reactions, the intracellular concentration of ATP is generally kept very constant at about 2-5 mM, depending on organisms and tissues, with a turnover rate of the ATP pool that is in the range of a few seconds (1). Hence, metabolic ATP generation in a cell must be balanced tightly with ATP-consuming processes. Small deviations from the standard cellular concentrations of free ATP, ADP, and AMP serve important regulatory roles in fine tuning this delicate balance.This balance between energy-consuming and -producing processes is particularly challenged in tissues that experience periods of high and fluctuating energy demand, such as brain, heart, or skeletal muscle. To maintain constant ATP levels, these tissues express creatine kinase (CK 1 ; EC 2.7.3.2) that uses creatine (Cr) to create a metabolically inert pool of phosphocreatine (PCr). Among other functions, this PCr pool serves as a temporal energy buffer that can replenish ATP rapidly during phases of high energy demand, according to the following reaction (2): MgADP Ϫ ϩ PCr 2Ϫ ϩ H ϩ i MgATP 2Ϫ ϩ Cr.

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Section: Discussionmentioning

confidence: 91%

Functional Expression of Phosphagen Kinase Systems Confers Resistance to Transient Stresses in Saccharomyces cerevisiae by Buffering the ATP Pool

Canonaco¹,

Schlattner²,

Pruett³

et al. 2002

Journal of Biological Chemistry

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“…ally causing severe cell damage (45,46) to the animal and its symbionts. It also is possible that the energy costs of maintaining cell pH over longer periods exceed the energy yield from fermentation alone, and the pH-regulation mechanism of one or both organisms of the holobiont eventually breaks down.…”

Section: Discussionmentioning

confidence: 99%

Mechanisms of damage to corals exposed to sedimentation

Weber

Beer

Lott

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

208

139

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We investigated the mechanisms leading to rapid death of corals when exposed to runoff and resuspended sediments, postulating that the killing was microbially mediated. Microsensor measurements were conducted in mesocosm experiments and in naturally accumulated sediment on corals. In organic-rich, but not in organic-poor sediment, pH and oxygen started to decrease as soon as the sediment accumulated on the coral. Organic-rich sediments caused tissue degradation within 1 d, whereas organic-poor sediments had no effect after 6 d. In the harmful organic-rich sediment, hydrogen sulfide concentrations were low initially but increased progressively because of the degradation of coral mucus and dead tissue. Dark incubations of corals showed that separate exposures to darkness, anoxia, and low pH did not cause mortality within 4 d. However, the combination of anoxia and low pH led to colony death within 24 h. When hydrogen sulfide was added after 12 h of anoxia and low pH, colonies died after an additional 3 h. We suggest that sedimentation kills corals through microbial processes triggered by the organic matter in the sediments, namely respiration and presumably fermentation and desulfurylation of products from tissue degradation. First, increased microbial respiration results in reduced O 2 and pH, initiating tissue degradation. Subsequently, the hydrogen sulfide formed by bacterial decomposition of coral tissue and mucus diffuses to the neighboring tissues, accelerating the spread of colony mortality. Our data suggest that the organic enrichment of coastal sediments is a key process in the degradation of coral reefs exposed to terrestrial runoff.

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“…Animals prone to experiencing regular periods of hypoxia in their natural habitat exploit a variety of mechanisms to cope with reduced oxygen availability (for review see Grieshaber et al, 1994). Tolerance to progressive hypoxia has frequently been determined by an analysis of the critical oxygen partial pressure (P ).…”

Section: Introductionmentioning

confidence: 99%

Metabolic performance of the squid Lolliguncula brevis (Cephalopoda) during hypoxia: an analysis of the critical PO2

Zielinski

Lee

Pörtner

2000

Journal of Experimental Marine Biology and Ecology

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Brief squid Lolliguncula brevis are regularly exposed to fluctuating oxygen levels in their shallow coastal environment. To assess hypoxia resistance, animals were exposed for two hours to ambient oxygen partial pressures (P ) between 19.3 kPa (normoxia) and 6.6 kPa (34.2% air O 2 saturation) at 20618C. In a second set of experiments, the animals were subjected to a low P of O 2 2.860.3 kPa (14.561.6% air saturation) for 15 to 60 min. Subsequently, metabolic, energy and acid-base status were analysed in the mantle tissue. Onset of anaerobic metabolism was observed between 9.4 and 7.9 kPa (48.7 and 40.9% air saturation), reflecting the critical oxygen tension for this species. The formation of octopine and acetate indicates a simultaneous onset of anaerobic metabolism in both the cytosol and the mitochondria during progressive hypoxia. Concomitantly, an intracellular acidosis developed. During exposure to oxygen partial pressures between 19.3 and 6.6 kPa, aerobic and anaerobic processes were sufficient to maintain energy status in the mantle musculature. No significant changes in ATP and phospho-L-arginine (PLA) concentrations were observed. In contrast, both ATP and PLA levels declined significantly after 15 min at an ambient P of 2.860.3 kPa. Concomitantly, the Gibb's free energy change of ATP hydrolysis fell to a O 2 21minimum value of about 244 kJ?mol , a level suggested to reflect limiting energy availability for cellular ATPases. These results indicate that hypoxia at 2.8 kPa (14.5% air saturation) rapidly takes Lolliguncula brevis to the limits of performance. However, it is probably capable of withstanding longer periods of moderate hypoxia close to 50% air saturation (9.7 kPa), enabling the squids to cope with oxygen fluctuations in their shallow estuarine environment or to dive into hypoxic waters by use of their economic jetting strategy. Nonetheless, the critical P is O 2 considered to be high compared to other hypoxia tolerant animals, an observation likely related to the high metabolic rate of these squids.

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Physiological and metabolic responses to hypoxia in invertebrates

Cited by 301 publications

References 261 publications

Functional Expression of Phosphagen Kinase Systems Confers Resistance to Transient Stresses in Saccharomyces cerevisiae by Buffering the ATP Pool

Functional Expression of Phosphagen Kinase Systems Confers Resistance to Transient Stresses in Saccharomyces cerevisiae by Buffering the ATP Pool

Mechanisms of damage to corals exposed to sedimentation

Metabolic performance of the squid Lolliguncula brevis (Cephalopoda) during hypoxia: an analysis of the critical PO2

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