2/4/11

Microbes: drivers of global biogeochemistry proportal.mit.edu 1/28/2011 Prochlorococcus marinus forces.si.edu Soil fungus Virginia Rich ‐ EEB Dennis Kunkel

Diatom

www.bioquest.org forces.si.edu Soil bacteria Termite prost www.nhm.ac.uk www.morning-earth.org/Graphic-E/ Biosphere/Bios-Microbe-Image/M- PCophryoscolex Rumen prost Ophryoscolex Coccolithophore

With material from Drs. Sco Saleska (U of Az), Gene Tyson (U of Queensland, Australia) and Kostas Konstannidis (Georgia Tech)

Outline I. Big Picture II. How do microbes make a living (and thus interact with biogeochemical cycles)? III. Microbes & the C cycle – the highlights A. Primary Producon B. Decomposion Soil respiraon, ocean respiraon IV. Menon of other cycles, & Summary

1 2/4/11

I. Big picture: microbes drive biogeochemical cycles

• ~ Half planetary primary marine forests & production (C fixation): microorganisms other big (cyanobacteria & green stuff phytoplankton)

• Organic matter degradation: Without microbial • Metabolic diversity:

recycling, nutrients Microbes perform all would be locked up & major metabolic become unavailable. pathways, and courses.worldcampus.psu.edu periodically reveal entirely new ones • Biomass: ~109 microbial cells/ (e.g. proteophodopsin, gram surface soil and ~106 cells/ml anaerobic methane oxidation). http://newscenter.lbl.gov/ seawater. (You have more microbial cells in your body than human cells). If all multi-cellular life disappeared 50-90% of marine biomass is microbial tomorrow the major biogoechemical (Census of Marine Life). cycles would likely proceed with very little change...

II. How do microbes make a living? • “Microbes” can mean several things!!! For this overview defined as single‐celled organisms: bacteria and archaea (together oen called the “prokaryotes”, also “microbes”) plus single‐celled eukaryotes (aka “protozoans”, and the majority of “prosts”) How are microbes involved in all these biogeochemical cycles? What do microbes – indeed all cells – need to make a living?

• CARBON for bulk of biomass • NUTRIENTS (N,P, S) and micronutrients for proteins, nucleic acids, etc. • WATER as a solvent (and a reactant in biomass producon) • ENERGY to allow them to work against entropy • ELECTRONS to transfer energy via redox reacons, and perform chemical transformaons – so a source and a sink for electrons ‐

2 2/4/11

Let’s take an example we’re more familiar with: us. In our special case, our foods (complex organic compounds) provide us with Carbon, with Bond energy, AND with electrons. How are organic compounds used for all these things? Recall the mitrochondria? (Which are, as you’ll recall from high school bio, descendents of free‐living bacteria that took up residence inside eukaryoc cells long ago). Mitochondrial electron transport chain

aka Krebs cycle

Wikipedia

Source for C, energy + electrons

= carbon compounds Mitochondrial electron transport chain Carbon compounds (= “food”)

www.power2fitness.com/images/krebs_cycle-lrg.gif

Wikipedia

3 2/4/11

Source for C, energy + electrons

= carbon compounds Mitochondrial electron transport chain Carbon compounds (= “food”)

biosynthesis biosynthesis

biosynthesis www.power2fitness.com/images/krebs_cycle-lrg.gif

Wikipedia

Mitochondrial electron transport chain Carbon compounds (= “food”)

ATP

biosynthesis biosynthesis

biosynthesis www.power2fitness.com/images/krebs_cycle-lrg.gif

Wikipedia

4 2/4/11

Mitochondrial electron transport chain Carbon compounds (= “food”)

ATP

biosynthesis biosynthesis

biosynthesis www.power2fitness.com/images/krebs_cycle-lrg.gif

Wikipedia

Mitochondrial electron transport chain Carbon compounds (= “food”)

ATP

biosynthesis biosynthesis

biosynthesis www.power2fitness.com/images/krebs_cycle-lrg.gif

Wikipedia

5 2/4/11

Mitochondrial electron transport chain Carbon compounds (= “food”)

ATP

biosynthesis biosynthesis

biosynthesis www.power2fitness.com/images/krebs_cycle-lrg.gif

Wikipedia

Mitochondrial electron transport chain Carbon compounds (= “food”)

ATP

biosynthesis biosynthesis

biosynthesis www.power2fitness.com/images/krebs_cycle-lrg.gif

Wikipedia Sink for electrons = O2 (producing water)

6 2/4/11

Words we use to describe where organisms get their carbon, energy, and electrons 1. Carbon • Autotroph Greek autos = self, trophe = nutrion. So what is their C source? How do they get it? What are some examples?

wikipedia proportal.mit.edu earthobservatory.nasa.gov • Heterotroph heteros = other, trophe = nutrion. So what is their C source? How do they get it? Examples?

Associated Press www.morning-earth.org/ Graphic-E/Biosphere/Bios- Microbe-Image/M- PCophryoscolex.jpg protistuser.uni- frankfurt.de.~schauder.ter mites.proto7_bg

2. Energy • Phototroph photo = light Energy comes from photons • Chemotroph chemo = chemical Energy comes from converng energy stored in chemical bonds (via their electrons) In both cases, captured energy is stored as ATP, carbs, lipids or proteins. 3. Electron Source • Organotroph organic = C‐containing. Use carbon compounds as electron donors. This includes us! • Lithotroph lithos = rock Use inorganic compounds as electron donors

4. Electron Sink

• Aerobic respiraon uses O2 as terminal electron acceptor. When it’s available, it gets used because of highly favorable energecs.

• Anaerobic respiraon occurs in absence of O2, using alternate ‐ terminal electron acceptor. E.g. denitrificaon uses nitrate (NO3 ), sulfate 2‐ reducon uses sulfate (SO4 ), methanogenesis uses carbon (CO2 or acetate)

7 2/4/11

Examples

• How would we be classified under this trophic nomenclature? – Get C from others – Get electrons from C compounds – Get energy from bond energy Therefore we are Chemo organo heterotrophs, as are

all mulcellular carnivores, herbivores, and many http://www.popartuk.com/g/l/lgsb0015+da-vincis-vitruvian- man-homer-simpson-the-simpsons-art-print.jpg many microbes. • How would land plants be classified? – Fix CO2 – Use sun for energy – What is their electron source? Is it organic or inorganic http://www.missouriplants.com/ Ferns/Equisetum_hymenale_stems Photo litho autotrophs not so important to memorize terms as to understand that a diversity of lifestyles exist, & thus a diversity of interactions with biogeochem. cycles

Many biogeochemical transformations are unique to Bacteria and Archaea, and not found in Eukaryotes, e.g.

Nitrogen fixation N2 ⇒ NH3

- - Nitrification NH3 ⇒NO2 ⇒NO3

Anaerobic respiration Use of electron acceptors

other than O2 Examples

Methanogenesis CO2 (or CH3COOH) ⇒ CH4

Denitrification NO - ⇒ N What jumps out just of this 3 2 brief sampling? The N cycle is dominated by 2- microbial transformations. Sulfate reduction SO4 ⇒ H2S

8 2/4/11

III. Microbes & the Carbon Cycle

Sco (and others) says:

“Carbon is the currency of life”:

photosynthesis

H2O + CO2  CH2O + O2

respiration Carbon in Reduced Carbon atmospheric CO2 in organic matter (biomass & energy supply)

A. Primary Producon aka autotrophy

Field et al. 1998 Science Ocean NPP Land NPP

earthobservatory.nasa.gov

≈

• Ocean NPP ~ land NPP. Much sparser biomass, so why? • The oceans cover a lot of territory (~71% of the earth’s surface) • Not a lot of mul‐cellular primary producers in the oceans – sea grasses & most seaweeds limited to coasts, etc. – so it’s all about the microbes

9 2/4/11

Who is doing this marine phototrophy? EUKARYOTIC 40-70% of ocean primary PHYTOPLANKTON production

proportal.mit.edu Dennis Kunkel CYANOBACTERIA www.nhm.ac.uk Coccolithophore (e.g. Prochlorococcus marinus) Diatom 30-60% of ocean primary production

earthobservatory.nasa.gov http://www.photolib.noaa.gov/ bigs/fish1880.JPG

But that’s just photoautotrophy… what about chemoautrophy? • In the oceans, chemoautrophy occurs in: – high organic‐maer coastal zone waters,

– oxygen minimum zones (low O2‐horizontal stretches of the oceans, the expansion of which is linked to climate change in several ways. “Dead zones” are an extreme anthropogenic type of oxygen minimum zone), – hydrothermal vent systems, – marine sediments, – marine basalts, – the water column of the open ocean,

– …. NSF press release for DeLong et al 2006 Science

Basically everywhere in the sea, to varying degrees

10 2/4/11

Example: Chemolithoautotrophs living on and below the sea floor on basalt.

“Laser confocal photomicrograph of a microbial biofilm aached to the surface of basalt chips from a depth of 1500 meters. Green is reflected light from the basalt surface and red is from Nile red–stained bacterial cells.”

Stevens & McKinley, 1995 Science.

Santelli et al., 2008 Nature Subseafloor microbes = 10–30% of the total living biomass of Earth - Whitman et al. 1998 PNAS.

How dynamic might these pools be? ANY data on SIZE of chemoautotrophic C fixaon? Very few. One elegant example in a deep‐sea, low‐carbon, open‐ocean habitat: Used carbon isotopes in microbial biomass to track autotrophy (“you are what you eat”). Ingalls et al., 2006 PNAS “Total [autotrophic] biomass producon by archaea in deep waters is ... 1% of annual marine primary producon... of a magnitude significant to the global carbon cycle and greater than... that buried in marine sediments.” (It’s on scale of 1/10th annual human C addion to atmosphere. What kind of chemoautotrophy? NH3 nitrification, by ammonia- oxidizing archaea (ammonia is electron DONOR) Walker et al., 2010 PNAS

11 2/4/11

Summary of microbial autotrophy

• Marine ~ terrerstrial NPP • Marine NPP ~ microbial

• Marine NPP = cyanos + earthobservatory.nasa.gov eukaryoc phytoplankton • But wait, there’s a lot of non‐ phoc habitat on the planet • Chemoautrophs are NSF for DeLong et al 2006 abundant and diverse • Unclear how much C they may be fixing Stevens & McKinley, 1995. Stevens & McKinley,

Microbes & the C Cycle: B. Heterotrophy • Hetero.s get their C from others: Microbes are master decomposers – predaon & herbivory of living ssues – scavenging of dead biomass MARINE • Results in breakdown of organic maer

TERRESTRIAL http://www.whoi.edu/cms/images/lstokey/ 2005/1/v40n2-honjo2en_4950.jpg

William S. Currie

http//berkeley.edu/news/media/ releases/2007/01/images/leaf_bags Stocker et al Cover of Science Feb 2010 https://courses.worldcampus.psu.edu/welcome/turf230/images/microbial

12 2/4/11

Microbial decomposion

• Provides energy for microbial growth (heteroTROPHY) • Releases nutrients

Vital for sustaining life

e.g. Recycled nutrients in ocean’s surface waters fuel 78% of marine primary producon (Duce et al 2008).

Microbial decomposion impacts climate www.bioquest.org

Soil bacteria • Influences ecosystem carbon storage and therefore climate.... • Respiraon = the measurable output of all life’s breakdown of organic maer (thus both autotrophic and heterotrophic respiraon.)

• CO2 is returned to the atmosphere by respiraon of mulcellular organisms and chemoorganotrophic microbes, plus anthropogenic acvies forces.si.edu Soil fungus

13 2/4/11

Terrestrial and marine respiraon

The Global C Cycle

IPCC 2007, Ch. 7; 1990s data

Values in black are natural, values in red are anthropogenic.

Soil respiration is the largest natural source of CO2 released to the atmosphere. Marine respiration isn’t far behind.

Both much larger annually than human addition of CO2 to atmosphere.

Terrestrial and marine respiraon

The Global C Cycle

IPCC 2007, Ch. 7; 1990s data

Values in black are natural, values in red are anthropogenic.

Soil respiration is the largest natural source of CO2 released to the atmosphere. Marine respiration isn’t far behind.

Both much larger annually than human addition of CO2 to atmosphere.

14 2/4/11

Terrestrial respiraon:

• In soils, the annual imbalance between plant photosynthesis and (plant + microbial) respiraon defines NEP = Net Ecosystem Producon = CO2 taken up by an ecosystem. • Soil respiraon = ~½ autotrophic (plant roots) and ½ heterotrophic (microbial + fungal decomposion) (e.g. Trumbore 2006 GCB)

Marine respiraon: • In oceans, the imbalance between production (+ terr. C input) and respiration defines the amount of C exported into the deep sea, where it has the potential to be buried and sequestered from the atmosphere. • e.g. in oceans, <0.1% of NPP reaches the sediment and gets buried (Falkowski & Oliver, 2007, Nature Rev. Micro.) • marine respiraon = ~20% autotrophic (phytoplanton) and 80% heterotrophic (microbes + metazoans) (e.g. del Giorgio & Duarte 2002 Nature) • of heterotrophic respiraon, metazoans account for <1% up to 50% depending on the region, producvity, depth, etc. (del Giorgio & Duarte 2002 Nature). Side Q: are fungi important decomposers in the oceans?

15 2/4/11

Variants on the basics (a): Microbial decomposion is a major process not only in soils & water, but in guts • Ruminants. Hard‐to‐degrade cellulosic plant materials require microbial enzymes – gut is like a microbial bioreactor…

• Termites. If you lived off gnawing wood,

you’d need help too – termite guts are filled www.morning-earth.org/Graphic-E/ Biosphere/Bios-Microbe-Image/M- PCophryoscolex with a rich community of symbioc microbes Rumen prost Ophryoscolex • Etc… Basically all mul‐cellular heterotrophs – including us… (your very own – likely unique to you! – commensal gut bacteria) forces.si.edu Termite prost

Variants on the basics (b): Non‐canonical heterotrophy

assigned reading http://www.mbari.org/twenty/images/proteo.jpg http://www.mbari.org/twenty/images/proteo.jpg Sll using organic carbon as their carbon source – so sll true heterotrophs – but geng addional energy from the sun or from inorganic chemical bonds. Inset example: proteorhodopsin.

16 2/4/11

Summary of microbial heterotrophy

• microbes are master degraders • releases nutrients • organic maer breakdown quanfied by respiraon • controls ecosystem C storage (imbalance between PP & respiraon) – also see Sco’s lecture 9/28 • soil resp. = ½ autotrophic + ½ heterotrophic • marine resp. = 1/5 autotrophic + 4/5 heterotrophic • decomposion is the major avenue of carbon loss from ecosystems, & is dominated by microbes • metazoan heterotrophy enabled by symbioc microbial decomposion in guts • biogeochemically important twists on heterotrophy where energy is supplemented from other sources.

Tip of the iceberg: Microbial “hands” in many biogeochemical cookie jars • Only had me to introduce the basic microbial C‐cycling phototrophy and heterotrophy • also drive the methane cycle as producers and consumers • Also drive the N cycle – Sco did thorough overview of N cycling on 9/30. As menoned, it’s all microbial. • And Fe cycling • And S cycling • etc…

17 2/4/11

Summary

I. Microbes have an amazing variety of metabolisms that place them at the focal transformaons of biogeochemical cycles II. Microbial (when incl. single‐celled eukaryotes) autotrophs perform ~50% of the primary producon on the planet III. Microbial heterotroph decomposers play a major role in terrestrial and marine organic maer degradaon

I. Respiraon is major source of CO2 to atmosphere II. Degradaon liberates accessible forms of nutrients

18