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