Why are Spartina grasses so successful? Adaptations to anoxia and hydrogen sulfide

Why are Spartina grasses so successful? Adaptations to

anoxia and hydrogen sulfide

Ray Lee and Brian Maricle

School of Biological Sciences

Washington State University

Spartina alterniflora and Spartina anglica

• Saltmarsh grasses native to the Eastern U.S. (S. alterniflora) and British Isles (S. anglica).

• Invasive species in Puget Sound and Willapa Bay in Washington State.

Why are physiological studies of Spartina relevant?

• Physiological processes are the link between environment and performance

Environment

Challengesopportunities

MetabolicStructuraladaptations

Physiologicalprocesses

Growthreproduction

Performance

Spartina are physiologically resilient and vigorous

• Physiological tolerance – Wide range of salinities– Waterlogged soils

• Anoxia

• Hydrogen sulfide

Distribution of hydrogen sulfide in sediments

Oxidized zoneNo hydrogen sulfide

Anoxic zoneHydrogen sulfide-rich

Sulfide is a potent toxin to aerobic respiration

• µM levels inhibit mitochondrial cytochrome c oxidase

• Sulfide binds to hemoglobin forming sulfhemoglobin

• Sulfide spontaneously reacts with oxygen producing hypoxic/anoxic conditions

• Can be used as an energy source by sulfide-oxidizing bacteria

Chemoautotrophic symbiosis

• An adaptation to exploit sulfide-rich environments

Tolerating anoxic sediments

• Aerenchyma

• Anaerobic metabolism– Alcohol

dehydrogenase

• Sulfide oxidation

Spartina anglica root

Functions of aerenchyma

• Oxygen transport

• Reduce cellular oxygen demands

Root Ultrastructure1 cm from root tip 2 cm from root tip

Root Ultrastructure4 cm from root tip 6 cm from root tip

Root Ultrastructure8 cm from root tip 10 cm from root tip

The difference in root structure between treatments of Spartina alterniflora

A comparison of root structure between treatments of Spartina anglica

S. anglica respirometry experiments

• Use automated flow-through respirometry system

• Investigate oxygen transport

Flow-through respirometry

mitochondria

O2

O2

O2

Root surface

Root - high O2 uptake

High oxygen consumption and/or low aerenchyma supply

mitochondria

O2

O2

O2

Root surface

Root - low O2 uptake

Low oxygen consumption and/or high aerenchyma supply

O2

O2

Oxygen transport is more effective in

S. anglica compared with S. alterniflora

Checking for oxygen transport

• A plant can be sealed into a flask of N2-flushed water.

• An oxygen-sensing probe can be used to monitor the water--any increase in O2 must have come through the plant.

Differences in oxygen transport between species

Negative fluxes=uptake; positive fluxes=release; n=9, 11, 9, 9

mitochondriaH2S

H2S

Root surface

Sulfide volatilization

Occurs in S. anglica but not S. alterniflora

Conclusions

• Function of increased aerenchyma appears to be to reduce oxygen demands NOT increase oxygen transport

• S. anglica has a highly effective oxygen AND sulfide transport system

Questions

• Can S. anglica grow better than S. alterniflora in anoxic/sulfidic conditions?

• Can sulfide levels ever be so high that plants cannot deal with it?

• What is the relationship between sulfide levels and effectiveness of eradication efforts?

Acknowledgements

• J. Doeller and D. Kraus (UAB)

• S. Hacker (WSU Vancouver)

• Kim Patten (WSU Long Beach)

• Miranda Wecker

• NSF, NOAA, WSU faculty seed grant

mitochondria

O2

H2S

SOxO2

O2

Enzyme orMetal catalystRoot surface

Sox mechanism

Spartina alterniflora roots catalyze the oxygenation of sulfide