Deep Secrets from the Marine Microbial Food Web

David Karl

SOEST

ACKNOWLEDGMENTS

Ed Laws /

Raleigh Hood

Joanie Kleypas

My lab

OUTLINE

Pre-JGOFS view of the marine microbial food web

New knowledge gained during JGOFS-era

Critical knowledge gaps

Future research prospectus

Slide 4

"THE IMMEDIATE TASKS OF MARINE MICROBIOLOGY" (KRISS, 1963)

Extension of at-sea observations and integration into "mainstream" oceanography, especially marine geochemistry

Year-round, repeat observations to resolve daily, seasonal and interannual variations

Estimation of productivity and determination of controls on P:B ratios

Begin systematic study of bacterial taxonomy, especially in "bathysphere" (i.e., deep sea)

Slide 6

R. W. EPPLEY, ca. 1984

PARADIGMS ca. 1985

Climax community in ocean gyres (McGowan, Hayward, Venrick et al.)

Fixed ecological stoichiometry

(Redfield et al.)

New (NO₃^-) and regenerated (NH₄⁺) production (Dugdale & Goering)

Export vs. PP (Eppley & Peterson)

Fixed subeuphotic zone remineralization (Martin et al.)

NOVEL MICROBES,
NOVEL ECOLOGIES

1988: Prochlorococcus (Chisholm)

1992: pelagic Archaea (DeLong/Fuhrman)

2000: rhodopsin-containing photoheterotrophs (Béjà and DeLong)

2000: rediscovery of anaerobic anoxygenic phototrophs (Kolber and Falkowski)

2002: SAR 11 (Rappé and Giovannoni)

2002 and beyond: ??

PROKARYOTE POWER

Large percentage of genome is devoted to metabolic regulation – large potential for "habitat tuning"

Direct exchange of "free DNA" (new genetic information) between and among otherwise unrelated prokaryotes (transformation) is commonplace in nature

"Species concept" uncertain

"Less than 1%"

Less than 1% of species

Only 1 "model" system

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WHAT SHOULD WE MEASURE?

DNA/RNA (genomics, community structure)

Cell numbers

Cell biomass (as C) and C-N-P

Metabolic activity, cell division, growth rate

Biomass production (as C)

Gross or net metabolic processes

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Slide 21

SOME NEW KNOWLEDGE GAINED DURING THE JGOFS-ERA

Microbial biodiversity -> biocomplexity and importance of community structure

Violation of "Redfield rules" of microbial production stoichiometry

Multiple nutrient co-limitation and P-Fe-N₂ syntrophy

Vitamin "ecology"

Slide 23

HOT CORE PARAMETERS

Systematic drawdown (by 70%) of inorganic-P over past decade

Systematic increase (by 50%) of N₂ fixation over past decade

Variable phytoplankton community structure, but

NO CHANGE IN PP!

Slide 25

Slide 26

"PRIMARY" PRODUCTION
(¹⁴C INCORPORATION) QUESTIONS

How important are non-carbon dioxide fixing phototrophs?

Why is PP constant despite large changes in community structure and nutrient inventories?

Why is PP uncorrelated with C-export?

What limits PP?

Is there a better method to estimate total bio-photo-energy flux?

Slide 28

A SEA OF DICHOTOMY

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DIVERSITY OF N₂ FIXERS
AT STA. ALOHA

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ECOLOGICAL STOICHIOMETRY: FROM REDFIELD TO FARFIELD

VITAMIN ECOLOGY

Most eukaryotes (especially diatoms) are vitamin (especially B₁, B₁₂) auxotrophs

Most prokaryotes (especially heterotrophic bacteria) can synthesize their own vitamins and then some

Vitamins (especially B₁ and B₁₂) are present in limiting concentrations in subtropical and Southern Ocean habitats

VITAMIN ECOLOGY

Vitamin bioavailability controls community structure

Vitamin syntrophy controls primary carbon fixation and export

Slide 40

Slide 41

JGOFS “MARCHING ORDERS”
REDUCING UNCERTAINTIES

To determine and understand on a global scale the processes controlling time-varying fluxes of carbon and associated biogenic elements

To develop a capability to predict the response of oceanic biogeochemical processes to natural and anthropogenic perturbations

Slide 43

EVERYTHING OLD IS NEW AGAIN!
JGOFS-SMP 2002

Taxonomy: Genome sequencing, bioinformatics, proteomics

Biochemistry: Novel energy transduction pathways, biodegradation of "recalcitrant" DOM

Physiology: N₂ fixation, anoxygenic phototrophy/photoheterotrophy, stoichiometry

Ecology: Symbiosis, niche partitioning, competition, natural selection

A FEW GUIDING PRINCIPLES
FOR THE FUTURE

Microbial DOES NOT = bacterial

Availability of field methods limits progress

Habitats are diverse and variable in space and time

Accurate models do not exist

POST-JGOFS CRITICAL KNOWLEDGE GAPS: MICROBIOLOGY/PHYSIOLOGY

Species ID and enumeration

Gene expression and regulation

Syntrophy/symbiosis/competition

POST-JGOFS CRITICAL KNOWLEDGE GAPS: ECOLOGY/BIOGEOCHEMISTRY

PP – flux – flux attrition

Plasticity of ecological stoichiometry

N₂ fixation – denitrification

Carbon AND energy fluxes

Compound-specific DOM analyses

R. W. EPPLEY, ca. 1984

D. M. KARL, ca. 2002

Slide 50


	Pre-JGOFS view of the marine microbial food web
	New knowledge gained during JGOFS-era
	Critical knowledge gaps
	Future research prospectus


	Extension of at-sea observations and integration into "mainstream" oceanography, especially marine geochemistry
	Year-round, repeat observations to resolve daily, seasonal and interannual variations
	Estimation of productivity and determination of controls on P:B ratios
	Begin systematic study of bacterial taxonomy, especially in "bathysphere" (i.e., deep sea)


	Climax community in ocean gyres (McGowan, Hayward, Venrick et al.)
	Fixed ecological stoichiometry
	(Redfield et al.)
	New (NO₃^-) and regenerated (NH₄⁺) production (Dugdale & Goering)
	Export vs. PP (Eppley & Peterson)
	Fixed subeuphotic zone remineralization (Martin et al.)


	1988: Prochlorococcus (Chisholm)
	1992: pelagic Archaea (DeLong/Fuhrman)
	2000: rhodopsin-containing photoheterotrophs (Béjà and DeLong)
	2000: rediscovery of anaerobic anoxygenic phototrophs (Kolber and Falkowski)
	2002: SAR 11 (Rappé and Giovannoni)
	2002 and beyond: ??


	Large percentage of genome is devoted to metabolic regulation – large potential for "habitat tuning"
	Direct exchange of "free DNA" (new genetic information) between and among otherwise unrelated prokaryotes (transformation) is commonplace in nature
	"Species concept" uncertain


	DNA/RNA (genomics, community structure)
	Cell numbers
	Cell biomass (as C) and C-N-P
	Metabolic activity, cell division, growth rate
	Biomass production (as C)
	Gross or net metabolic processes


	Microbial biodiversity -> biocomplexity and importance of community structure
	Violation of "Redfield rules" of microbial production stoichiometry
	Multiple nutrient co-limitation and P-Fe-N₂ syntrophy
	Vitamin "ecology"


	Systematic drawdown (by 70%) of inorganic-P over past decade
	Systematic increase (by 50%) of N₂ fixation over past decade
	Variable phytoplankton community structure, but
	NO CHANGE IN PP!


	How important are non-carbon dioxide fixing phototrophs?
	Why is PP constant despite large changes in community structure and nutrient inventories?
	Why is PP uncorrelated with C-export?
	What limits PP?
	Is there a better method to estimate total bio-photo-energy flux?


	Most eukaryotes (especially diatoms) are vitamin (especially B₁, B₁₂) auxotrophs
	Most prokaryotes (especially heterotrophic bacteria) can synthesize their own vitamins and then some
	Vitamins (especially B₁ and B₁₂) are present in limiting concentrations in subtropical and Southern Ocean habitats


	Vitamin bioavailability controls community structure
	Vitamin syntrophy controls primary carbon fixation and export


	To determine and understand on a global scale the processes controlling time-varying fluxes of carbon and associated biogenic elements
	To develop a capability to predict the response of oceanic biogeochemical processes to natural and anthropogenic perturbations


	Taxonomy: Genome sequencing, bioinformatics, proteomics
	Biochemistry: Novel energy transduction pathways, biodegradation of "recalcitrant" DOM
	Physiology: N₂ fixation, anoxygenic phototrophy/photoheterotrophy, stoichiometry
	Ecology: Symbiosis, niche partitioning, competition, natural selection


	Microbial DOES NOT = bacterial
	Availability of field methods limits progress
	Habitats are diverse and variable in space and time
	Accurate models do not exist


	Species ID and enumeration
	Gene expression and regulation
	Syntrophy/symbiosis/competition


	PP – flux – flux attrition
	Plasticity of ecological stoichiometry
	N₂ fixation – denitrification
	Carbon AND energy fluxes
	Compound-specific DOM analyses