Hyperbaric Tolerance Flashcards
All known marine organisms are vertically constrained within distinct bathymetric strata.
What factors may be causing some organisms to have larger bathymetric ranges than others?
- The factors that set these limits remain elusive as the effects of (covariables) temperature, pressure, salinity, oxygen, habitat availability and type and food supply are often covarying.
- Hydrostatic pressure is the most conspicuous environmental gradient in the sea, and we can see significant physical effects of hydrostatic pressure on proteins and lipoprotein membranes
- reaching ~1000atm (100MPa) in the hadal zone (6,0000 -11,000m)
What are the significant physical effects of hydrostatic pressure on proteins and lipoprotein membranes?
When you chill a lipid down, it is essentially a fat, and it’s going to become more solid. The loss of flexibility in the membrane effects its ability to manage those exchanges of water and solutes across the barrier.
Hydrostatic pressure does a similar thing, proteins are at risk of becoming denatured and the pressure forces water into the hydrocarbon backbone of the protein structure, causing it to unfold.
- Deformation leading to functional change (Barstow et al. 2008, PNAS 105: 13362-13366)
- Subunit dissociation and denaturing of enzymes (Winter & Dzwolak, 2005, Phil. Trans. R. Soc. A 363: 537-562)
Hyperbaric tolerance in marine fauna
Is there a pressure-sensitive equivalent to heat shock proteins and managing exchange of solutes to mitigate the effect of salinity?
- Macromolecular proteins such as cytoskeleton tubulin and actin are dissociated affecting cell morphology and organisation
- This occurs at pressures as low as tens of MPa in shallow-water organisms
- Lipid bilayers of biological membranes are one of the most pressure-sensitive molecular components (Macdonald, 1997, Comp. Bioch. Physiol. A 304: 47-58)
- Increased pressure reduces flexibility in lipids, the function of various nucleic acids and the catabolism of carbohydrates (Balny et al., 2002, Bioch. Biophys. Acta 1595: 3-10)
- The two covarying gradients of temperature and pressure effects can interact
- The pressure increase of 10 MPa is equivalent to temperature decrease of 13-21oC (depending on membrane composition)
- A temperature increase of 2.8oC can reverse the reduction in membrane fluidity imposed by the pressure of 10 MPa
- Interesting in global warming scenarios, would a deepening of the thermocline allow some animals to go deeper? (if they can manage the pressure)
Ben study looking at some of the issues around the associated covariance of temperature and pressure.
This was actually done by a Newcastle student, Andrew Oliphant. He was looking at some of the issues around the associated covariance of temperature and pressure and looking to see whether you can find evidence in common shallow-water animals and find evidence of their ability to extend their ranges beyond where you would normally find them.
- Common estuarine shrimps were out into experimental pressure chambers, and they were able to monitor aspects of their performance over time.
- Data looks at the total movement of the animal (taking different movements, such as the beating of the antenna. Active movement occurs if they are physically moving about.
- Loss of equilibrium - the point the shrimps ‘give up’ lose the ability to move
- The experiment was run at four different temperatures (30, 20, 10 and 5 degrees)
- The point 50 % lost equilibrium occurs at different pressures dependant on what temperature the animals are held at.
- Laemonetes varians showed an increased sensitivity to pressure with decreasing temperature; however, shrimp were capable of tolerating hydrostatic pressures found outside their normal bathymetric distribution at all temperatures.
- ‘Loss of equilibrium’ (LOE) in ≥50% of individuals was observed at 11 MPa at 5°C, 15 MPa at 10°C, 20 MPa at 20°C and 21 MPa at 30°C.
- Low rates of oxygen consumption were observed at 5 and 10°C across all pressures, from 10 to 30°C, the rate of oxygen consumption increased with temperature.
Oliphant et al. (2011). J.Exp.Biol. 214: 1109-1117
Identifying the effects of hydrostatic pressure on the bathymetric zonation of all deep-sea species is an unrealistic task
Examining trends across large groups of species is possible – for example elasmobranchs and ray-finned bony fishes (Actinopterygii)
Now that scientific investigations are reaching full ocean depth some extreme depth limits for life in the marine biosphere are emerging (Jamieson et al., 2010. Trends Ecol. Evol. 25(3): 190-197)
Two of these recent limits are;
Two of these recent limits are;
- Absence of elasmobranchs from below ~4,000m
- Absence of all fishes from below ~8, 200m (only 2 families have been found deeper than 6,000m)
Why is there an absence of sharks from the abyssal oceans? case study.
Case study – Priede et al. (2006). The absence of sharks from abyssal regions of the world’s oceans. Proceedings of the Royal Society B, 273: 1435-1441
Analyses a large dataset from trawl data to put forward some ideas about why we might see an absence of sharks in the abyssal ocean.
Elasmobranchs are in black and teleost distribution is in grey. Deepest fish was a Harriota spp at 3,010m (rabbitfish)
- Longline fisheries, set by the Norwegians between 400 - 4200 m, and the deepest shark found was 3280m (Bathyraja pallida, Centrophorus squamosus Ray and cookie-cutter shark)
- Baited camera traps, 400- 5900m, deepest elasmobranch was a ray (benthic associated and not as actively swimming as some of the larger sharks) at 3996m. The deepest shark was the Portuguese dogfish at 2490m.
Absence of sharks from the abyssal oceans
Case study - metanalysis
MDO records for 669 species of Chondrichthyes (elasmobranch - black); 8691 Actinopterygii (bony fishes -grey)
- Deepest elasmobranch - close to 4000
- Deepest fish - much deeper.
- With exception of 7 species, Chondrichthyes restricted to <2,500m
- 260 species of bony fish from several families >2500m
- Is body size the main factor? Looked at the relationship between the rate of species loss and depth.
- using just data for fish the same size as elasmobranchs different presents a different trend
- something fundamentally different
So what explanations could there be for the absence of sharks in the abyss?
- Species number
- Body size
- Water temperature
- Pressure
- Buoyancy
- Metabolism
So what explanations could there be for absence of sharks in the abyss?
Species number
Diversity metric
Species number – simply probability that bony fish more likely to produce species capable of surviving deeper waters
However, if you consider the difference in the rate of decline and give both species a similar extinction rate, sharks would be expected to reach 7,500m
So what explanations could there be for absence of sharks in the abyss?
Body size
Body size – the clear metabolic advantage of size for scavengers, so larger size of sharks should have an advantage
- metabolic advantage of size for scavengers
*
So what explanations could there be for the absence of sharks in the abyss?
Water temperature
Water temperature – shouldn’t be a barrier, intermediate water masses could cue orientation to optimum depth – sharks also absent from abyssal Mediterranean (isothermal).
Not physiologically capable of managing dome of these colder temperatures.
So what explanations could there be for the absence of sharks in the abyss?
*Pressure
Pressure- unlikely to be a physiological barrier as Chrondrichthyes have high concentrations of protein stabiliser compounds in their body fluids.
So what explanations could there be for the absence of sharks in the abyss?
Buoyancy
All the other factors do not explain the difference, so have to look at other physiological differences
Is there any potential, competitive advantage for going deeper, related to how they manage their buoyancy?
- deep-water sharks have large, lipid-rich squalene livers
- For 1kg buoyancy; 7.14kg squalene energy content of 264MJ
- Most successful scavenger/predator in deep water is a ray-finned bony fish - Coryphaenoides armatus – swim bladder.
- Using gas entails a pumping cost at 4000m of 90kJ
- Even with 5-10% efficiency, the energy cost of using gas is trivial compared with a lipid-based system
So what explanations could there be for the absence of sharks in the abyss?
Metabolism
How does squalene vs swim bladder relate to variability in their metabolism?
- Metabolism decreases as you go down through the ocean – much higher activities in bathyal (1,000-3,000m) compared to abyssal species linked to a decrease in the food supply
- Priede et al. (2006) proposed
- Absence of sharks likely linked to the absence of truly low energy forms
- Large energetic penalties of lipid-rich livers may be decisive in excluding Chondrichthyes from the abyss
case study to explain why there is an absence of fishes below 8200m.
Case study – Yancey et al. (2014). Marine fish may be biochemically constrained from inhabiting the deepest ocean depths. PNAS 111 (12): 4461-4465
Did his earlier work on osmolytes, then started working on whether there is some evidence for osmolytes being responsible for biochemical depth limitation in fishes.
- He proposed the mechanism for pressure adaptation in fishes would involve a compound, which he named ‘piezolytes’
- Small organic solutes that counteract pressure effects on proteins
- Allow proteins to work over greater depth ranges but constrain species depths if regulation is limited
- What are they?
- He found that the osmolytes he had been studying has piezolyte qualities – intracellular chemical effectors that prevent osmotic water loss
- Extracellular fluids are dominated by NaCl; cells accumulate osmolytes to achieve osmotic balance
Which osmolyte may be important for extending depth capabilities?
If you look shallow-water species, osmolytes tend to be from a sweet of compounds, neutral amino acids - things like glycine and taurine bases. But also a lot of them use more complex methyl amines
One of the main ones found in a lot of organisms is trimethylamine N-oxide (TMAO).
Yancey et al. (2014). started looking into TMAO, its function and how it may interact with other proteins. Hypothesised that if TMAO was an important osmolyte, and inferred protein in relation to depth.
- A potent protein stabiliser found to counteract the effects of pressure on enzyme kinetics and protein stability
- Alters water structure in a way that reduces the tendency of pressure to force water molecules into proteins
- pressure trying to force water molecules into the protein and break apart hydrocarbon backbone, and TMAO slows this down, reducing the effect of denaturing.
- Osmophobic effect (repels water)…………….And it makes fish smell fishy!!
- Many deepwater species found to have elevated levels of TMAO in their body fluids
Kelly, R.H. & Yancey, P.H. (1999). Biological Bulletin 196: 18-25 What does this paper show a
Range of different groups. Can see broad categories of shallow, abyssal and bathyal populations. The TMAO content is always higher in the abyssal populations.
Kelly, R.H. & Yancey, P.H. (1999). Biological Bulletin 196: 18-25
What does this graph show?
TMAO is of a higher concentration in deeper organisms
There is also more urea
What has TMAO got to do with the 8200 m mark?
- One of the functions of TMAO is as an osmolyte
- most vertebrates are osmoregulators – being very hypoosomotic to seawater
- Shallow -water fishes low levels of osmolytes – TMAO 40-50 mOsmolkg-1
- Deep-water fishes show a striking correlation between TMAO and depth of capture (261 mOsmolkg-1 at 4,850m
- Yancey et al. (2014)
- Piezolyte hypothesis – TMAO is increasingly needed at greater depths.
- Depth-limit hypothesis – TMAO accumulation results in physiological osmotic maximum near observed depth limit. There is a point where the cells cannot accumulate any more TMAO.
- Because ou are accumulating TMAO to protect themselves from the effect of pressure, yet in doing so you are interrupting the iron balance between the extracellular fluids in the body and the external medium. There will become a point when the fish is completely isoosmotic - if you continue to change the solute concentration you will flip from hypo to hyperosmotic.
- Based on the osmolarity of muscle fluid and the accumulation of TMAO Yantze’s theory predicts a maximum depth of 8200, - the point at which TMAO concentration in the body would be equal to the seawater.
what alternative theory exists for chondrichthyes?
When compared to bony fishes, elasmobranchs use urea as an osmolyte.
Urea is damaging (perturbs) proteins at high concentrations, to get around this sharks use urea with methylamines like TMAO in a 2:1 ratio.
As they go deeper they rely less on urea and more on methylamines, as pressure and urea puts a lot of pressure on proteins.
At a midpoint, around 1500 m the levels of TMAO in sharks starts to level out.
Laxson et al. (2011). Decreasing Urea: Trimethylamine N-Oxide ratios with depth in Chondrichthyes: A physiological depth limit?. Phys. Biochem. Zool. 84 (5): 494-505
This study suggests that the accumulation of TMAO sets the depth limits for many sharks.
Effect of pressure on copepods.
Descending copepods subjected to low temperatures and increased pressure
Significant additive effects on the composition of membrane phospholipid fatty acids (PLFAs)
DHA {22:6 (n-3)} moiety increased with pressure is greater at colder temperatures – maintains membrane fluidity and confers tolerance
Copepods cannot synthesise DHA
