Berenbrink CAREX Viterbo 2009 Web Version

8/12/2019 Berenbrink CAREX Viterbo 2009 Web Version

1/20

From deep sea fish to diving birds and mammals:

Challenges to the O2 transport systems of polar

vertebrates

Michael Berenbrink

Viterbo, June 2009


2/20

The buoyancy problem

Brown algae Portuguese man-of-war Chambered nautilus Lovely hatchet fish

Most tissues of marine organisms are denser than the surrounding medium

must continuously spend energy to avoid sinking

or incorporate appropriate amounts of less dense materials gas floats are most efficient

flexible gas floats are compressed with increasing depth

needs to be countered by swimming movements

or needs gas secretion against high pressure to maintain neutral buoyancy

Sea otter


3/20

Aims

- understand themechanistic (proximate)

cause of a physiological

phenomenon:

"How does it work?"

- and the ultimate (evolutionary)

cause:

"Why does it work this way?"


4/20

Swimbladder Anatomy in a Deep Sea Fish

Lovely hatchetfish

Argyropelecusaculeatus

At night: 100 - 300m

During day: 300 - 600m


5/20

Vein

Swim-

bladder

capillaries

rete mirabile

up to 80% O2at pressures up to 90 atm

Schematic blood supply to Swimbladder

Swim-

bladder

epithelium

Swimbladder

Artery


6/20

Oxygen tension (mmHg)

HbO2Saturation

(%)

R. W. Root (1931)

5.5

6.0

6.5

7.0

7.58.0

8.5

0

100

150

0

How to release O2 from the blood?

The Root effect

pH


7/20

Species differences in the Root effect

10 nM 100 nM 1 M 10 M

50

60

70

80

90

100

Haemolysate H+activity

HbO2(%)

8 7 6 5

Xenopus

Freshwater

butterflyfish

African

knifefish

African lungfish

Elephantnose fish

Catfish

Bichir

pH

HbO2 saturation (%)

in air equilibrated Hb solutions

Berenbrink J. Exp. Biol. 210: 1641 (2007)


8/20

Mechanism for O2 Secretion

Vein

Rete mirabileArtery

Swim bladder

epitheliumTissuecapillaries

HbO2

HbO2H+

Root

Effect

O2+Hb

O2O2O2

Hb

3 Key

components:- Acidification

- Root Effect

- Rete mirabile

How did

they evolve?

After Berenbrink J. Exp. Biol. 210: 1641 (2007)


9/20

10

20

30

40

50

60

70

80

Root

effect

(%)

Reconstructing Root effect

evolution

After Berenbrink et al. Science 307: 1752 (2005)


10/20

10

20

30

40

50

60

70

80

Root

effect

(%)


evolution



11/20


12/20

Scyliorhinus

Mustelus

Squalus

Protopterus

Lepidosiren

Xenopus

Sus

Homo

Erpetoichthy

s

Polypterus

Acipenser

Lepisosteus

Amia

Scleropages

Pantododn

Xenomystus

Campylomormyrus

Gnathonemu

s

Anguilla

Megalops

Clupea

Danio

Cyprinus

Leuciscus

Tinca

Misgurnus

Pangio

Botia

Gyrinocheilu

s

Brycinus

Apteronotus

Synodontis

Pelteobagrus

Oncorhynchus

Esox

Gadus

Synbranchus

Mastacembe

lus

Platichthys

Scomber

Dicentrarchu

s

Perca

Reconstructing Swim Bladder Rete Mirabile Evolution

Sharks

Lungfis

hes

Tetrapo

ds

Teleosts

Ray-finned Fishes

?? ? ? ?

Swim bladder retia

mirabilia and O2 secretion

evolved at least 4 times

independently



13/20

Time (Mya)

0 50 100 150 200 250 300 350 400 450

Rooteffec

t(%)

0

10

20

30

40

50

60

70


evolution

Atmospheric oxygen

concentration (%)

(Berner, 2007)

Swimbladder

rete mirabile Ocular

rete mirabile


14/20

7.88

7.40

6.90

6.26

5.26

Human Hb A

modified from Lukin & Ho (2004)

Ray-finned fish Hb

The Root effect may have evolved initially for the same purpose as the Bohr effect

Both effects show 'aberrant' features at very low pH

These may have subsequently been selected for in ray-finned fishes


15/20



16/20



17/20



18/20


19/20

Conclusions

Understanding of physiological mechanisms needs an integrative approach

across multiple levels of organisation

This may be best achieved in model species

True understanding of genetic adaptation needs a phylogenetic framework and

thus comparative approach across species

Because it works at the organism/environment interface, the oxygen transport

system of vertebrates is ideally suited for studies of environmental adaptation


20/20

Acknowledgements

Everybody who generously donatedspecies samples

bbsrcbiotechnology and biological sciences

research council

Liverpool Pia Koldkjaer

Scott Mirceta

Andy Cossins

Berlin Oliver Kepp

Documents

Berenbrink CAREX Viterbo 2009 Web Version