FAUNAL PHYSIOLOGICAL ADAPTATIONS IN HYDROTHERMAL VENT COMMUNITIES

1
FAUNAL PHYSIOLOGICAL ADAPTATIONS IN HYDROTHERMAL
VENT COMMUNITIES

• 18 November 2009
• Megan Vaughan, Megan Guest, Meade Humble

2
Introduction

• - Recap ? Biomass trends in the deep sea
  Biomass generally decreases with depth, until it
  is 1 as that of the surface at 4km Food intake
  Most organisms in the deep sea depend on
  photosynthetically derived material from surface
  waters Major divisions Organisms divided into
  epifauna and infauna deep sea dominated by
  Echinodermata and Arthropoda

3

• ? discovery of hydrothermal vents (due to
  strange chemical and thermal readings) changes
  many of these assumptions
• - Vents have extreme environmental conditions
  organisms must find ways to cope with drastic
  changes in temperature, pressure, lack of light,
  toxicity, dissolved oxygen

4
Fauna of Hydrothermal Vents

• - Molluscs ? both very big compared to other
  deep-sea species occupy crevices
• ? Calyptogena magnifica
• ? Bathymodilus thermophilus ? can have densities
  of 10 kg/m2 influences names of vent sites
  (Mussel Bed and Clambake) has a mouth and gut,
  unlike most vent species, so may also get some
  nutrient flux from surface productivity lower
  levels of enzymatic activity in gill tissues may
  mean more independence from symbionts than other
  species

http//www.mbari.org/molecular/images/mussels.jpg
http//www.ifm-geomar.de/fileadmin/ifm-geomar/allg
emein/avillwock/meeresonline/calyptogena.jpg
5

• - Worms
• ? Riftia pachyptila ? also anchored in
  crevices placed within class Vestimentifera
  gills not just for respiration, but also to
  collect food for symbionts more tolerant of
  anoxia because of presence of haemoglobin (?)
  C.magnifica tends to avoid settling with Riftia,
  but other species use tube as extra habitat
• ? Alvinella pompejana ? a polychaete tend to
  be found around hotter of vents (150-350C) form
  honeycomb-like tube masses seem to cultivate
  and eat bacteria more than use symbiosis
• ? Saxipendium coronatum ? draped over rocks
  on vents in Galapagos could be suspension feeders

http//www.bioweb.uncc.edu/biol2120/Images/Riftia.
jpg
6

• - Crustaceans
• ? Crabs (including Cyanograea praedator,
  Bythograea thermydron) ? live among Riftia tubes
• ? Shrimp (Alvinocaris lusca)
• - Others ? anemones, fish, larvae, copepods

http//open.live.bbc.co.uk/dynamic_images/natureli
brary_626/downloads.bbc.co.uk/earth/naturelibrary/
assets/b/by/bythograeidae/bythograeidae_1.jpg
http//farm1.static.flickr.com/6/6488639_995a41607
2.jpg?v0
7
Symbiosis

• - Whole vent community supported by
  chemoautotrophic bacteria oxidize sulphur
  compounds from vent fluid fix organic carbon
  from CO2 and CH4
• - Can influence distribution of hosts around
  vents depend on redox reactions to get
  energy/nutrition and therefore must lie between
  vent fluid and ambient water

8

• - Both molluscs and worms contain huge numbers of
  symbionts within their tissues C.magnificas
  gills are 75 bacteria, and so is a third of
  Riftias body weight!
• ? Belkin et al (1986) found that bacteria in
  Riftia can synthesize sulfide and not
  thiosulfate, but for Bathymodiolus, it was
  opposite.

http//www.hydrothermalvent.com/php/symbiosis/174-
424.html
9
Belkin et al, 1986
10
Chemosynthesis

• - Chemosynthesis The pathway by which bacteria
  in hydrothermal vent communities synthesize
  complex organic molecules from hydrogen sulphide
  gas and dissolved carbon dioxide

4H2S CO2 O2 ? CH2O 4S 3H2O
Allaby, A. and Allaby, M. (1999) Chemosynthesis
The Dictionary of Earth Sciences, Acessed online
12 Nov 2009
11

• - Cavanaugh et al (1981) ? bacteria in Riftia
  mostly contained in an organ called a trophosome
  contains sulphur granuoles was previously
  found that APS reductase and ATP sulfurylase
  (enzymes that produce ATP from oxidizing sulphur)
  were in high concentrations in trophosomal tissue

http//www.divediscover.whoi.edu/images/biology-an
atomy.jpg
12
Hydrogen Sulfide

• H2S, HS-, S2-
• Oxidation produces high amounts of energy

Hydrogen Sulfide
Sulfate
Elemental Sulfur
Sulfite
http//filebox.vt.edu/users/chagedor/biol_4684/Cyc
les/Soxidat.html
13
Hydrogen Sulfide

• H2S extremely toxic
• Inhibits cytochrome-c oxidase

http//vcell.ndsu.edu/animations/etc/first.htm
14
Hydrogen Sulfide

• Dissolved sulfide reacts spontaneously with
  oxygen and other oxidants to form less reduced
  compounds
• Vent fauna must sequester and transport sulfide
  to the trophosome while preventing poisoning or
  oxidation

15
Sulfide Uptake and Transport

• Acidic vent water ? H2S
• Physiological pH 7.5 (H2S HS-)

Morel (1983)
16
Sulfide Uptake and Transport (R. pachyptila)

• Diffusion of H2S limited
• (mechanism?)
• HS- principal sulfure
• species at physiological
• pH
• HS- taken up by the
• tubeworm binds rapidly
• to hemoglobin

http//bugs.bio.usyd.edu.au/learning/resources/Pol
ychaetes/riftia1.htm
17
Goffredi et al. (1997)
HS-
H2S
18
Hemoglobin

• Hemoglobin transports HS- and O2 to the
  trophosome
• Sulfide cannot react with O2 or inhibit aerobic
  respiration when bound to hemoglobin
• High affinity for both HS- and O2 (no competition
  for O2 binding site)
• High concentrations in the vascular blood
• Three types V1 (3500 kDa), V2 (400 kDa), and
  C1 (400 kDa)
• V1 can bind 3X more sulfide

19
Fisher et al. (1988)
20
Oxygen

• Endosymbiotic bacteria require high
  concentrations of O2
• O2 binds to hemoglobin, maintaining a partial
  pressure gradient and reducing sulfide oxidation
• Temperature Effects
• Hemoglobin affinity for O2 decreases at higher
  temperatures

21
R. pachyptila
Wittenberg et al. (1981)
22
Temperature

• Vent fauna are adapted to extreme temperatures
• E.g. Alvinellid polychaetes are likely the most
  thermotolerant hydrothermal-vent metazoans

A. pompejana
http//absentmag.org/issue02/html/simon_dedeo.html
23
A. pompejana (Pompeii worm)
Cary et al. (1998)
Start Recording
Recover Probes
24
A. pompejana (Pompeii worm)

• Not possible to measure body temperature in situ
• Methods obtain inaccurate results due to the
  nature of the worm and its tube

Chevaldonne et al. (2000)
25
Thermal Adaptations
Dahloff et al. (1991)

• Enzymes remain active at higher temperatures

26
Thermal Adaptations

• High numbers of linker chains in hemoglobin
• Thermostability of rDNA

http//www.cadilapharma.com/cadila/business.htm
27
Dixon et al. (1992)
Warmer Habitat
Cooler Habitat
28
Growth Rates

• Giant Tubeworm (Riftia) colonized new vents
  following volcanic eruption, 9N EPR
• Tube length increased at rate gt 85 cm yr during
  1st year of growth
• Sexually mature within 2 years
• Smaller tubeworm (Tevnia jerichonana), colonized
  same site, with GR gt 30 cm yr, reaching full size
  within one year

(Lutz et al. 1994)
29
Growth Rates

• Clayptogena Magnifica Bathymodiolus
  thermophilus
• Radiochronometry, direct measurement of shell
  growth and shell dissolution techniques
• 0.5 to 4-6 cm y?1 depending on technique, size,
  and site

30
Energy Metabolism

• Hand Somero 1983
• Non-vent organisms have low rates of metabolism,
  an adaptation to low food availability
• Can rich food supply support high metabolism of
  vent species even in the presence of Hydrogen
  Sulfide?
• HS inhibitor of Cytochrome-c oxidase aerobic
  respiration
• Compared enzyme activity of energy metabolism
  pathways
• Glycolysis
• Citric Acid (Krebs) Cycle
• Electron transport chain
• For Vent spp., and shallow-living
  marine spp.

31
Enzyme activity
Hand and Somero (1983)
32

• Hand Somero (1983)
• Results
• Enzyme activity in vent tissues qualitatively and
  quantitatively similar to related shallow-living
  species
• Types of metabolic pathways and flux rate
  through pathways are similar to non-vent
  organisms.
• Rates of Primary production by chemolithotropic
  bacteria at vents may be high enough to sustain
  metabolic rates comparable to shallow water
  animals in food rich environments
• Cytochrome c oxidase activity comparable, despite
  high HS
• Except clam which may rely on anaerobic
  metabolism
• Adaptation to HS toxicity must depend on other
  physiological adaptations

33
Sulfide Detoxification

• Sulfide insensitive systems
• Exclusion of H2S
• Symbiont Consumption
• Sulfide binding
• Amino Acid Metabolism
• Peripheral Internal Defense
• Epibionts
• Tubes Cuticles

34
Sulfide Detoxification

• Sulfide insensitive hemoglobin cytochrome-c
  oxidase systems
• Only Riftia have sulfide insensitive hemoglobin
• Exclusion of H2S
• Active exclusion through membrane (only in
  Riftia)
• Symbiont Consumption
• Endosymbiotic bacteria oxidize sulfide as an
  energy source
• Sulfide binding
• Binding of Sulfide to render it inactive
• Tubeworms, bind sulfide to hemoglobin
• Clam, sulfide binding factor (Arp et al. 1983)

35
Sulfide Detoxification

• Amino Acid Metabolism
• (Brand et al. 2007)
• Protection from and/or transport of Sulfide
• Hypotaurine
• high in all tissues
• Thiotaurine (Hypotaurine Sulfide)
• Vent mussels have unusually high concentrations
  of the amino acid thiotaurine compared to
  shallow-water, non-symbiont bearing mussels
• Vent tubeworms and clams also have high levels of
  thiotaurine
• Thiotaurine contents increase during sulfide
  exposure in symbiont-bearing tissues
• Rxn is reversible, stores sulfide, released as
  endosymbionts deplete free sulfide

36
Amino Acid Metabolism

• Varying levels of Thiotaurine represent
  differences in sulfide levels
• Environmental sulfide levels
• Dependency on amino acid detoxification

(Brand et al. 2007)
37
Sulfide Detoxification

• Peripheral Internal Defence
• Sulfide oxidizing activities in superficial cell
  layers of non-symbiotic species
• Epibionts
• Sulfide-oxidizing chemoautotrophic activity
• Precipitate sulfide bound to minerals
• Tubes Cuticles
• Act as Barriers to diffusion of sulfide

http//oldsite.dri.edu/deesprojects/alison_VEEG.ht
m
38
Heavy Metal Detoxification

• Metallothinein
• Metal-binding protein
• Common in specific tissues of vent organisms
• Polychaetes store metals in membrane bound
  vesicles
• Riftia
• highest concentrations found in trophosome
• A. Pompejana (Pompeii worm)
• metallothinein associated with dorsal epidermis
  and digestive system
• Paralvinella sp
• mucus (Containing metallothionein-like proteins)
  sheds inorganic particles from surface

39
Heavy Metal Detoxification

• C. magnifica (vent clam)
• Intracellular granules in kidney cells,
  eventually excreted
• Crustaceans
• Incorporate trace elements in exoskeleton
• Loose metals during molting

40
Additional References

• Brand, G.L., Horak, R.V., Le Bris, N., Goffredi,
  S.K., Carney, S.L., Govenar, B., Yancey, P.H.
  2006. Hypotaurine and thiotaurine as indicators
  of sulfide exposure in bivalves and
  vestimentiferans from hydrothermal vents and cold
  seeps. Marine Ecology. 28 (1) 206-216.
• Dahloff, E., OBrien, J., Somero, G. N., Vetter,
  R. D. 1991. Temperature effects on mitochondria
  from hydrothermal vent invertebrates Evidence
  for adaptations to elevated and variable habitat
  temperatures. Physiol. Zool. 641490-1508
• Dahloff, E., J., Somero, G. N. 1991. Pressure and
  temperature effects on mitochondria dehydrogenase
  of shallow- and deep-living marine invertebrates
  Evidence for high body temperatures in
  hydrothermal vent animals. J. Exp. Biol. 159
  473-487
• Dixon, D. R., Simpson-White, R., Dixon, L. R. J.
  1992. Evidence for thermal stability of ribosomal
  DNA sequences in hydrothermal vent organisms. J.
  Mar. Biol. Assoc. U.K. 72 519-527.
• Fisher, C. R., Childress, J. J., Sanders, N. K.
  1988. The role of vestimentiferan hemoglobin in
  providing an environment suitable for
  chemoautotrophic sulfide-oxidizing endosymbionts.
  Symbiosis 5 229-246.
• Godfredi, S. K., Childress, J. J., Desaulniers,
  N. T., Lallier, F. H. 1997. Sulfide acquisition
  by the vent worm Riftia pachyptila appears to be
  via uptake of HS- rather than H2S. J. Exp. Biol.
  200 2609-2616.
• Morel, F. M. M. 1983. Principles of Aquatic
  Chemistry. John Wiley Sons, New York, 446 p.
• Van Dover, C. L. 2000. Physiological ecology. In
  The Ecology of Deep-Sea Hydrothermal Vents.
  Princeton University Press, Princeton, pp.
  183-208.
• Wittenberg, J. B., Morris, R. J., Gibson, Q. H.,
  Jones, M. L. 1981. Hemoglobin kinetics of the
  Galapagos rift vent worm, Riftia pachyptila Jones
  (Pogonophora Vestimentifera). Science 213
  344-346.