Ecology of Subm erged Cenotes in Lake
Huron: P layers and P rocesses
Bopi Biddanda1,
Stephen Nold2, Steve Ruberg3
Scott Kendall1,
1Grand
Valley State University
2University of Wisconsin - Stout
3NOAA Great lakes Environmental Research Lab
A NSF & NOAA funded, TBNMS & NOF supported study
Submerged sinkholes along a increasing
depth/decreasing sunlight gradient
3
2
1
What are the production processes?
Biddanda et al. 2009 (Eos)
1. El Cajon Bay Springs (shallow)
Shallow El Cajon
Springs
Groundwater Emerging from Shallow Submerged Sinkhole
Springs (White arrows) are characterized by green algae
(Green arrows) and purple cyanobacteria (Purple arrows)
Green Algae
Purple Cyanobacteria
El Cajon Spring_0001.wmv
2. Middle Island Sinkhole (Low-Light: 5-23 m)
Benthic Cyanobacterial Mats
Dominant Purple Colored Mats
Cyanobacteria Under Microscope
Potential for both
Oxygenic and
Anoxygenic
Photosyntheisis?
Red autofluorescence
of chlorophyll
Purple and Green Filaments
Anoxygenic Photosynthesis (Cyanobacteria)
H2S + CO2 = CH2O + SO42-
3. Isolated Sinkhole (Aphotic) 93m
Nepheloid layer over Sinkhole a Biogeochemical hotspot
Microbes in the Nepheloid layer
White Benthic Mats on lake floor
(Similar to Marine Vents and Seeps!):
Biddanda et al 06 (Ecosystems) S-oxidizing chemosynthetic bacteria?
Isolated Clip_0001.wmv
Comparison of Lake Huron water and
sinkhole vent water.
Parameter
Lake Huron
Conductivity (mS/cm)
0.2
Dissolved Oxygen (mg/L)
11
Temperature (oC)
seasonal
pH
8.3
Chloride (mg/L)
6
Sulfate (mg/L)
15
Venting GW
2.3
< 0.3
~9
7.1
25
1250
Ruberg et al. 2009 (MTSJ)
Microbial Processes in Huron Sinkholes:
Changing Light Gradient
QUESTION/HYPOTHESIS
Photosynthesis in
Shallow waters shifts to
Chemosynthesis in
Deep water(?).
El Cajon sinkhole 1m
Full Sunlight
Middle Island Sinkhole 20 m
5-10% Sunlight
Isolated Sinkhole 93m
No Sunlight
Metabolic Studies in El Cajon
Preliminary Observations: Benthic photosynthesis is
the major production process in shallow sinkholes
Metabolism Studies at El Cajon Spring from June 11-13, 2007
6.3
Night
Day
Day
Day
Night
5.8
Water
5.3
Benthic 2
4.8
Benthic 3
4.3
3.8
3.3
2.8
2.3
1.8
1.3
0.8
17
:3
0
15
:0
0
12
:3
0
10
:0
0
7:
30
5:
00
2:
30
0:
00
21
:3
0
19
:0
0
16
:3
0
14
:0
0
11
:3
0
9:
00
6:
30
4:
00
1:
30
23
:0
0
18
:0
0
-0.2
20
:3
0
0.3
Time (Military Time)
Question: What is the fate of the excess benthic primary production?
Low Light
Middle Island Sinkhole
Environment
Dark and light experimental benthic chambers over microbial mats
Preliminary Observations: Oxygenic Photosynthesis
is not adequate to balance C in deeper sinkholes
Benthic Metabolism Studies on Purple Mats in MI
Sinkhole on July 24-26, 2007
5
Day
Night
Day
Night
Day
4
3.5
3
2.5
2
1.5
Benthic Dark
1
0.5
Benthic Light 1
Time (Military Time)
Question: Can Anoxygenic Ps and Chemosynthesis
account for the apparent C deficit in deeper sinkholes?
11
:1
5
8:
45
6:
15
3:
45
1:
15
10
:1
5
12
:4
5
15
:1
5
17
:4
5
20
:1
5
22
:4
5
7:
45
5:
15
2:
45
0:
15
0
14
:1
5
16
:4
5
19
:1
5
21
:4
5
Dissolved Oxygen (mg/L)
4.5
14
Production Processes Study: C-Bicarbonate
Incorporation into Benthic Mats-Sediment under
in situ conditions
Experimental Design:
SUNLIGHT
Sediment
Cores
Incubation
Chamber
Over-view
DARK
Oxygenic
Chemosynthesis
Photosynthesis
Anoxygenic
Live,DCMU
Photosynthesis and Killed
Controls
(+DCMU)
DCMU inhibits Oxygenic Ps
Cyanobacterial
Mat on sediment
Surface
Incubation
Chamber
Front View
Autotrophic Production Processes at Shallow and Deep Sinkholes:
Observation: Shift from Photosynthesis to Chemosynthesis
Production Process
El Cajon
Mid Island
Isolated
Spring
Sinkhole
Sinkhole
µgC/L/d
µgC/L/d
µgC/L/d
__________________________________________________________
Oxygenic Photosynthesis
67 (24)
~30 (5)
NA
Anoxygenic Photosynthesis
0
22 (6)
NA
Chemosynthesis
21 (5)
10 (6)
20
62
20
Total Autotrophic Production 88
_________________________________________________________
OBSERVATIONS
Dominant Autotrophic
Production Process
Oxygenic
Photosynthesis
Oxygenic & Anoxygenic
Photosynthesis
Changing Light Gradient
El Cajon sinkhole (1 m)
Full Sunlight
Middle Island Sinkhole (20 m)
5-10% Sunlight
Chemosynthesis
Isolated Sinkhole (93 m)
No Sunlight
Hypothesized Scenarios of Production Processes in Sinkholes
Oxygenated Lake
Huron Water
Anoxic, Sulfate-rich
Groundwater
Oxygenic
Photosynthesis
(Green Algae)
Chemosynthesis
(Microorganisms)
Anoxygenic
Photosynthesis
(Cyanobacteria)
Purple, green and white microbial mats over rocks
Sediment Core
0
Mat
Structure
Color
Dominant
Organisms
0
Purple
Filamentous
Cyanobacteria
10
White
Filamentous
Sulfur oxidizers
15
White
Crystalline
Carbonate
layer
Diatoms,
Nematodes,
Ciliated Protists,
Tardigrades
0.4
0.6
20
25
0.2
Black,
OrganicRich Muck
Methanogens
0.8
Depth (cm)
Depth (cm)
5
Bacteria: 16S rRNA Clone Library Composition
Verrucomicrobiales
δ-Proteobacteria
1%
Chloroflexi
1%
1%
ε-Proteobacteria
Firmicutes
3%
1%
γ-Proteobacteria
3%
β-Proteobacteria
5%
CFB
7%
Cyanobacteria
78%
Middle Island sinkhole Mat (0-0.5 cm)
Archaea and Eukarya
C
SSU rRNA clone library composition
Arthropoda 18%
Nematoda 5%
Alveolata 5%
Platyhelminthes 3%
Ciliophora 3%
Crenarchaeota 9%
Tardigrada 2%
Fungi 1%
Plasmodiophorida 1%
Other 10%
Chlorophyta 1%
Rhizaria 1%
Euryarchaeota 49%
Unc. bacterium 1%
α-Proteobacteria 1%
Middle Island sinkhole, 7-9 cm
MicroEukaryotes
SSU rRNA clone library composition
Nematoda
14%
Tardigrada
14%
Arthropoda
7%
Ciliophora
65%
Middle Island sinkhole, 0-0.5 cm
Comparing Lake Huron Benthic Mats to
Other Systems of the World
Lake Hoare, Antarctic Dry Valleys
Dale T. Andersen
images.spaceref.com/astro/lter/sm0207.JPG
Lake Huron, Michigan
Lake Cadagno, Switzerland.
A Submerged Cenote in Laguna Bacalar, Mexico
What’s Inside?
A Submerged Sinkhole in Lake Huron, Michigan
Microbes & Carbon
Look Similar?
Observations
• Submerged sinkhole ecosystems in Lake Huron are characterized by
physicochemical gradients,and microbially dominated processes.
• There is emerging support for the “Variable Production Process
Gradient Hypothesis” in sinkholes: Oxygenic Photosynthesis in sunlit
shallow waters shift to Chemosynthesis in aphotic deep water
sinkholes.
Questions
• With their low oxygen and high sulfur content, are Lake Huron’s
sinkhole ecosystems similar to marine vents, terrestrial S springs,
submerged cenotes,and Antarctic lakes?
• What is the fate of benthic mat production and the source of
sedimentary carbon?
• Potential for discovery of novel organisms and processes - Case for
protection/preservation of these unique habitats?
Institutional Support: GVSU, UW-Stout,
Thunder Bay National Marine Sanctuary, NOAA and Noble Odyssey Foundation.
Underwater diver photography: Russ Green, Luke Clyburn and Tane Casserley
Underwater ROV videos: Steve Ruberg and Guy Meadows
Aerial photography: Scott Kendall and Bopi Biddanda
Funding: NSF Microbial Interactions and Processes Program
NOAA-Office of Ocean Exploration
More info: Bopi Biddanda: [email protected] or visit - www.gvsu.edu/wri