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Promotionskolloquium
Rita Dunker15. December 2010
Motility of the giant sulfur bacteria Beggiatoa in the marine environment
General Introduction
Temperature response of gliding motility in Beggiatoa
Patterns of gliding motility in Beggiatoa
Summary & Outlook
Outline1
The Genus Beggiatoa
-Proteobacteria
Large, multicellular filaments
Form mats on soft sediment surface or live within the sediment
Store elemental sulfur (S0) in the cytoplasm
Oxidize reduced sulfur compounds with oxygen or nitrate
Auto- or heterotrophic nutrition
→ Link the S-, N- and C-cycle of sediments
Introduction
From
Tesk
e a
nd
Nels
on
, 2
00
6
Small marine Beggiatoa
Freshwater Beggiatoa
Vacuolate sulfur bacteria(Large marine Beggiatoa, Thioploca, Thiomargarita)
1 cm
50 µm
2
Habitats of Beggiatoa:
Coastal environments:
Sediments of bays, fjords, inter- and subtidal zone
Organic material
Photosynthetic microbial mats
and deep sea hotspots like
Seepage areas (cold seeps, mud volcanos..)
Geothermally active areas
Whale falls
Introduction T response Motility patterns Summary
Imag
e c
ou
rtesy
of
Han
s R
øy
© A
WI/I
frem
er
5 cm
3
Sediments with Beggiatoa occurrence
Soft sediment
Opposing gradients of oxygen and sulfide
Sediment surface if oxygen and sulfide overlap
Suboxic zone if oxygen and sulfide are separated
→ Habitats with fluctuating conditions
→ Beggiatoa constantly need to reorient in their environment
Red
raw
n f
rom
D
un
ker,
20
05
Red
raw
n f
rom
Jø
rgen
sen
et
al. 2
01
0
Introduction T response Motility patterns Summary4
→ Gliding motility is crucial for the positioning of the filament in the environment
→ Tactic responses provide cues for the directed movement
Oxic
Anoxic
1 mm
From
Lark
in a
nd
Hen
k,
19
96
Motility in Beggiatoa
Locomotion by slime extrusion through pores
Tactic responses to chemical and physical stimuli
Introduction T response Motility patterns Summary
From: Møller et al. 1985
Oxic
Anoxic
5
Beggiatoa mat on the sediment surface
45% → 95% air saturation, 40 h, 30 fps
Introduction T response Motility patterns Summary6
1 cm1 cm
1 cm
45% air sat. 95% air sat.
Questions
Does temperature control the gliding speed of Beggiatoa ?
Is the speed of gliding motility adapted to the prevailing temperature of different climatic locations?
What is the acclimatisation potential of gliding speed to changing temperatures?
Temperature response of gliding motility7
Background
Beggiatoa occur at all climates:
Permanently cold, temperate, tropical
Oftentimes seasonally fluctuating temperatures
Growth and metabolism are temperature dependent, how about gliding motility?
Minimum Temperatur
e
Optimum Temperatur
e
Maximum Temperatur
e
Introduction T response Motility patterns Summary8
Mod
ified
aft
er
Dale
et
al.
20
08
Annual temperature in 2004
275
280
290
TSWI
(K)
jan feb mar apr may jun jul aug sep oct nov dec
.
18°C
3°C
Methods:
Tropical, temperate and arctic filaments
Temperate filaments acclimatized to summer and winter conditions, respectively
Custom-made chamber for monitoring of gliding speed of single filaments
Temperature control by a thermostat
Introduction T response Motility patterns Summary9
The temperature range for gliding
Introduction T response Motility patterns Summary
tropical temperate summer
temperate winter
arctic
Dunker et al. 2010
10
MotilityRespiration
from
Rid
gw
ay a
nd
Lew
in,
19
88
tropical temperate summer
temperate winter
arctic
Calculation of
Range for optimal physiological activity
Activation energy
Arrhenius equation
Introduction T response Motility patterns Summary11
T range for gliding wider that range for optimal physiological activity
T in situ within the range for optimal physiological activity
Optimum T beyond the range for optimal physiological activity
Extended T range at winter conditions
RT
EA
alnln
Du
nke
r et
al.
20
10
T in situT opt
Response at the extreme ends of the temperature range
Filaments withstand transient freezing
Decrease in gliding speed at the cold end is reversible
Decrease in gliding speed at the warm end is irreversible
Introduction T response Motility patterns Summary12
Arctic filaments
Temperate filaments
Conclusions:
Gliding speed regulated by T
Gliding is a physiologically regulated response
Gliding speed is adapted to the prevailing environmental T → ubiquitous distribution of Beggiatoa
Acclimatisation to seasonal T changes on a community scale
Introduction T response Motility patterns Summary13
Motility patterns in Beggiatoa
Questions
Which gliding patterns do Beggiatoa filaments use to orient in their environment?
Can these patterns explain the Beggiatoa distribution in the suboxic zone?
14
Methods
Filaments in gradient agar tubes
Imaging setup with illumination and interval imaging option
Image analysis
Monitoring of
Single trails
Changes in gliding direction
Introduction T response Motility patterns Summary15
Trails of filaments
Within the mat: Filaments „anchor“ at the overlap of oxygen and sulfide
Above and below the mat: Filaments glide long trails, move a net distance away from their origin
How?
Introduction T response Motility patterns Summary16
Du
nke
r et
al. s
ub
mit
ted
Reversal patterns of filaments
Within the mat: Average distance is shorter than filament length
Above and below the mat: Average distance glided is longer than filament length
Filaments change reversal behaviour when gliding into the mat
Introduction T response Motility patterns Summary
Du
nke
r et
al. s
ub
mit
ted
17
Introduction T response Motility patterns Summary18
Beggiatoa mat in an oxygen sulfide gradient, 4 h 30 min, 25 fps
Modeling Beggiatoa motility
Filament in the mat
Filament above and below the mat („random gliding“)
Introduction T response Motility patterns Summary19
Can the model explain the observed Beggiatoa distribution in a photosynthetic mat with a diurnal migration pattern?
Introduction T response Motility patterns Summary20
Red
raw
n f
rom
Hin
ck e
t al.
20
07
dusk dawn
Introduction T response Motility patterns Summary
→ 10 h of darkness is not enough to follow the migrating oxygen front
21
Modeled biomass distribution
Counted biomass distribution
Red
raw
n f
rom
Hin
ck e
t al.
20
07
dusk dawn
10 h dark cycle
Introduction T response Motility patterns Summary
Most random trails less than a day
Long random trails:
NO3- storage is
gradually depleted
Trail duration: several days
→ High biomass in the suboxic zone
→ High NO3- storage
capacity needed
NO3-NO3-NO3-NO3-NO3-NO3-NO3-NO3-NO3-
22
Beggiatoa distribution in the suboxic zone
Conclusion
Increase of reversal frequency keeps filaments at the oxic-anoxic interface
Long random trails can bring filaments back to the oxic-anoxic interface
High NO3- storage capacity fuels the long random trails in
the anoxic sediment
Phobic responses protect the filaments from gliding out of the suboxic zone
Introduction T response Motility patterns Summary23
Summary and Outlook
Beggiatoa gliding speed underlies T control
→ mechanism of gliding?
Beggiatoa distribution in suboxic zone is in accordance with a phobic response to sulfide
→ nature of the response to sulfide?
→ role of sulfide in mat formation?
Reversal behavior
→ coordinated? cell-to-cell communication?
Introduction T response Motility patterns Summary24
Thanks to:
Prof. Dr. Bo Barker Jørgensen
Dr. Hans Røy
Dr. Tim Ferdelman
Dr. Anja Kamp
Dr. Jan Fischer
Associate Prof. Dr. Lars Peter Nielsen (Uni Århus)
Dr. Peter Stief
Dr. Dirk de Beer
Dr. Heide Schulz-Vogt
Technical staff:
Electronic workshop
Mechanic workshop
Biogeochemistry group
Microsensor group
My colleagues from the Biogeochemistry group, family and friends
Thank you for your attention
Introduction T response Motility patterns Conclusion
From
: M
ølle
r et
al.
19
85
NO3-
S0
H2S SO42-
H+
Nitrate transport:
H+ translocation ATPase
H+ translocating pyrophosphatase
NO3-/H+ antiporter
Carbon metabolism:
Autotrophic or heterotrophic
Large marine strains: RubisCO
Sulfur utilisation:
H2S, S0, S2O3-
Poly-phosphate storage as by genomic data
Vacuole
Cytoplasm
Introduction T response Motility patterns Conclusion
Model of the gliding mechanism in
Myxobacteria Hydration of electrolyte gel
fibers
Gel expands and leaves through the opening of the pores
Yields enough propulsion force to explain gliding motility at the observed speed
Wolgemuth et al. 2002
Introduction T response Motility patterns Conclusion
The temperature range of physiological adaptation
Arrhenius function:
ln = ln A - Ea/RT
Arrhenius plots:
Calculation of the activation energy Ea
Ea gives an estimate of the T dependence of a reaction
Similar Ea to that of bacterial enzymatic processes from cold environments
tropicaltemperate summer
temperate winter arctic
Introduction T response Motility patterns Conclusion
Origin of filamentsT response of gliding speed
Tin situ
(°C)
Topt
(°C)
Ea (kJ
mol-1)Q10 source
Tropical Mesophilic 20 37 49 2.1 (19-29 °C) this study
Temperate Mesophilic 13 30 58 2.3 (12-22 °C) this study
Temperate (cold acclimatized)
Mesophilic 4 30 50 2.1 (8-18 °C) this study
Arctic Psychrotolerant 6.5 17 46 2.0 (0-10 °C) this study
Gliding motility of Beggiatoa alba
35.2 Crozier and Stier, 1926
Gliding motility of Oscillatoria
38.7 Crozier and Federighi,
1924
Gliding motility in Oscillatoria princeps
30-40 42 144a) Halfen and Castenholz, 1971
Gliding motility of Flexibacter polymorphus
35 61.13 2.06 (15-35 °C) Ridgway and Lewin, 1988
Respiration of Flexibacter polymorphus
40 58.62 2.64 (15-35 °C) Ridgway and Lewin, 1988
Introduction T response Motility patterns Conclusion
Average distances:
Do individual reversal frequencies match the mat position?
Within the mat: Filaments glide shorter distances
Above and below the mat: Filaments glide longer distances
Introduction T response Motility patterns Conclusion
Motility in Beggiatoa below the mat- a random walk?
Diffusion coefficient D of a filament below the mat:
tD 4 L
t 4/L D 2
Filaments without a cue move as by a random walk
Introduction T response Motility patterns Conclusion
Solid line: Distance moved away from the origin as observed in a real filament
Dashed line: Distance of a particle diffusing at the D of a Beggiatoa filament
Dotted line: Distance moved away from the origin of a modeled Beggiatoa filament
Introduction T response Motility patterns Conclusion
• Nitrate storage: 270 mM• Nitrate consumption: 13 mM/day → lasts 21 days
Introduction T response Motility patterns Conclusion
Introduction T response Motility patterns Conclusion
Can the model help to explain the distribution pattern of Beggiatoa in the suboxic zone?
Known parameters of coastal sediment from Århus Bay
Frequency analysis plot:
Most random trails less than a day
Time spend on random trails: on average 10 days
→ Duration of random trails depends on NO3
- storage
Du
nke
r et
al. s
ub
mit
ted
Introduction T response Motility patterns Summary
Reversal behavior of Beggiatoa
10 µm
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