Diversity and Ecology of Autotrophic
and Mixotrophic Microbes in the
Ocean
Summary
Bach et al., 2006, EOS, Feb 14th
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Revised view of processes occurring in the
open ocean
•Oxygenic photosynthesis by
cyanobacteria and
phyotoplankton by far
dominant process
•Tends to be limited by
nutrients, not energy
•However, ocean contains light
dependent metabolic types
not expected before
•Microbes in the ocean are
more flexible than previously
thought, blurring the
distinction between
autotrophs and heterotrophs
Karl et al., 2002 Nature 415:590-591
•Chemolithoheterotrophs?
Chemolithoheterotrophy
• Organisms that can use OC as C-source and inorganic
chemicals as energy source
• Silicibacter pomeroyi as an example
• Belongs to Roseobacter clade within α-Proteobacteria
• Very versatile metabolism
– Can supplement energy need by oxidizing CO and/or
reduced inorganic S and organic sulfur
• Strategy is probably widespread in open ocean, as
comparison w/ Sargasso Sea shot gun library shows
Moran et al., 2004 Nature 432:910-913
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Role of Autotrophic Crenarchaeota in Deep Ocean
?
• Uncultured crenarchaeota dominate biomass in deep ocean
• Indications that at least some might be autotrophs
3
• First isolated mesophilic
Crenarchaeon
• First report of archaeal
nitrification
• Carbon Fixation Pathway?
Francis et al., PNAS 2005
Is archaeal autotrophy based on NH4+oxidation widespread in Ocean?
• Widespread occurrence of archaeal amoA in different
oceanic provinces: quantification and expression?
• Evidence for autotrophic DIC-fixation in different regions:
Atlantic, Pacific
• Biomass potentially produced by autotrophic Archaea
appears to be significant:
– Larger than carbon buried in marine sediments
– Same magnitude as methane production
• Also evidence for uptake of OC
– However, in situ analyses indicate that 71% of produced carbon
derives from autotrophy
• Mixotrophy or metabolic diversity among different
crenarchaeaota?
– NH4+-oxidizers confined to redox-cline?
Ingalls et al., PNAS 2006
• Other energy sources for chemolithoautotrophy?
4
Initial
water
Candidatus
Cenarchaeum
symbosium
Incubation at 27˚C
Arabian Sea
1000 m
water
column
Arabian Sea
surface
Incubation sediment
at 13˚C
Damste et al., 2002
Ingalls et al., 2002
Wuchter et al., 2004
• Interesting GDGT distribution:
• In surface water crenarchaeol (peak 2) is by far dominant GDGT
• In deep water GDGT-O (peak 1) is dominant
• Temperature effect?
• Ratio between GDGT-0 and crenarchaeol seems to correlate with temperature
• Would have been nice to complement lipid data with 16S rRNA and amoA data
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•Processes in deep-marine sediments
mainly driven by degradation of
photsynthetically dervide organic
matter
•Autotrophs recycle material
– Methanogens
– Acetogens
•Oxidants delivered from basement?
– Indicating low metabolic activity
in basement?
•Novel metabolism by archaea
– Using OM as carbon source
– Methane oxidation for
generating energy
DeLong, Nature 2005
• Multiple lines of evidence used to
assess “active” component of
microbial community
– rRNA
– FISH
– FISH-SIMS
– Intact-Phospholipids plus CSIA
• Archaea dominate active fraction
• No sign that methane is
incorporated into biomass
• Hypothesis: Used for energy
generation alone
Methane
DIC
FISH-SIMS
IPL’s
TOC
• C comes form refractory OM ->
fermentation?
• Indicates extremely low
maintenance energy requirements
(magnitudes lower to what is known
from lab cultures)
• Very slow turnover (100 - 2,000 a)
Biddle, Lipp et al., PNAS 2006
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Subsurface biosphere in oceanic crust is potentially extensive:
•Diagram of mid-ocean ridge, ridge flank and ocean basin
•Zones that differ in their relative exchange between ocean water column and
basement can be differentiated:
•Active exchange: Ridge Axis (I), unsedimented ridge flank (II), exposed
rocky outcrops (IV)
•Isolated: sedimented ridge flanks with sediment thickness >160 m
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Ridge Flanks are important
• 70-80% of heat flux occurs on ridge flanks
• Important for chemical fluxes: mobilization and precipitation
• Ridge flanks 1-65 Ma make up 70% of ocean basins
• Potentially enormous habitable volume on a global scale
• Significant potential for chemolithoautotrophic production in
crust (<20Ma): same magnitude as heterotrophic processes in
deep marine sediments
– Basalt weathering through iron- and sulfur oxidizers
(aerobically and anaerobically)
– H2-oxidation driven by hydrolysis of basalt
• Subsurface biosphere off-axis might be more extensive and
active than that on-axis!
• Weathering of crust exposed at ocean floor potentially also
supports chemolithoautotrophic processes -> Iron oxidizers!
• Role of mixotrophs or chemolithoheterotrophs?
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What is driving deep-sea hydrothermal vents:
Hydrogen, sulfur, iron?
Chemolithoautotrophic systems tend to be energy limited
Always true? What about macro- and micronutrients?
Can full potential always be utilized?
Need for experimental data
Autotrophic Carbon Fixation at Vents:
There is more than the Calvin cycle!
Chimneys + Sub-Surface:
•rTCA, reductive acetyl-CoA pathway,
Calvin Cycle, hydroxypropionate pathway?
Surface:
•Symbionts: Calvin Cycle, rTCA
•Free-living autotrophs: rTCA, Calvin Cycle
Needed are studies that couple identity with function and
rate measurements!
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Are Hydrothermal vents net autotrophic or heterotrophic?
Karl, 1995
Where to go from here?
• Chemoautotrophic carbon production in the Ocean is currently
poorly constrained
–How much is produced and by which pathway?
–Role of mixotrophy and lithoheterotrophy?
• How do mass and energy transfer between pelagic ocean, the
benthos, and the ocean crust affect the distribution and activity
of oceanic prokaryotes?
• Thermodynamic calculations and models provide guidance, but
ultimately measurements are needed!
• Multidisciplinary approaches needed to obtain further insights
–careful coordination between theory, experiment, and observation
–isotopic distributions, mixed and pure cultures, genotypes, patterns of
gene expression, inorganic and organic geochemical data, and
distributions of biomarker lipids
• Incorporate new findings into models
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Future Challenges
• Inability to culture:
• Limited scope of metabolic potential
• What is minimum maintenance energy?
• Cultivation remains ultimate goal!
• Linking identity with function and rates!
• Measure activities in situ
• Low biomass <-> Contamination
• Inaccessibility
• Sensitivity and availability of sensors and analytical tools
• Interdisciplinary education
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