Microbial Pathways in the Sea

1. Microbial Pathways in the Sea What is the relative importance of bacteria and viruses in regulating the flow of energy and the cycling of nutrients in marine ecosystems?

2. New and rapidly expanding field... History is relevant to understanding how other marine ecological processes (e.g., fisheries yield models) are influenced by microbes.

3. HISTORY 1950’s: Relatively large photosynthetic prokaryotes were recognized as important in Nitrogen cycling (e.g., Trichodesmium) • Traditional plate assays for counting bacteria indicated about 103 bacteria ml-1. • Approximately equal (numerically) to phytoplankton • Small size (100x smaller than phyto) suggested they were of minimal importance ecologically.

4. HISTORY Late 1960s: Advent of new membrane filtration products allowed careful size-fractionation. Pomeroy and Johannes (1968) Size-fractionated respiration (oxygen demand) greatest at < 5 um Importance over-looked... Compare to earlier smallest ‘net’ sizes of 20 um!!

5. HISTORY Subsequent fluorometry of bacterial cells in 1980s showed an incredible under-estimation of bacterial concentrations in the sea... Not 103 ml-1, but 106-108 ml-1 !! ~5 orders of magnitude more abundant than phytoplankton! Bacteria concentrations are relatively constant world-wide.

6. Why are bacteria so successful in the sea? • High Carbon conversion (growth) efficiencies (around 80%) • High production rates -- doubling times usually less than phytoplankton (up to several doublings per day)

7. Where does the Dissolved Organic Carbon (DOC) required by bacteria come from? Constant supply of dissolved organic substrates from phytoplankton Estimated ~50% of phytoplankton production is required to fuel bacterial requirements • In the surface layer, phytoplankton DOC comes from: • Exudation of organic material from cell during rapid growth • ‘Autolysis’ -- self-rupturing of cell contents • ‘Sloppy feeding’ by metazoans

8. At depth (below photic zone), DOC derived mostly from sinking detrital material. Up to 80% of sinking organic materials can be solubilized and consumed by bacteria associated with ‘marine snow’ Highest concentration of bacteria in the sea is on ‘marine snow’

9. Other nutritional requirements of bacteria... Nitrogen Phosphorus Sulfur In other words, bacteria compete directly with phytoplankton for nutrients

10. Special cases... Bacteria that reduce Nitrogen and Sulfur compounds derive oxygen from bound sources (i.e., oxidized compounds like nitrate and sulfate). These bacteria are obligate anaerobes since presence of oxygen will cause the spontaneous oxidation of reduced compounds. Where would you expect to find ‘denitrifying’ bacteria in the sea?

11. Special cases... Chemoautotrophy Some bacteria derive energy to ‘fix’ CO2 from reduced compounds such as hydrogen sulfide (H2S). Where would we expect to find chemoautotrophic bacteria?

12. Uptake Rate Concentration Bacteria are competitive for substrates with phytoplankton. Bacterial advantages: • High growth rates -- bacteria respond rapidly, and are tightly coupled with supply of dissolved nutrients • Chemotaxis-- can direct their movements toward the highest concentration of nutrients • Multiple transport systems for dissolved substrates enhances uptake over wide range of concentrations Bacteria will out-compete phytoplankton for N and P, especially at low concentrations

13. Phytoplankton Fish Zooplankton Ciliates (5-20 um) Bacteria (0.2-2 um) Flagellates (1-5 um) In oligotrophic environments (mid-ocean gyres) • Decomposer biomass > Producer biomass • Protozoans (flagellates and ciliates) graze heavily on bacterial production • ‘Locks’ nutrients up in this recycling system • Prevents losses to deep sea (DOM) ‘Microbial Loop’

14. The Microbial Loop (Azam et al. 1983)

15. Infection of bacterial and phytoplankton by VIRUSES Important source of cell lysing is by viral infection 50% (perhaps more?) of bacterial mortality due to viruses • Marine viruses (discovered in late 1980s): • Non-living, non-cellular particles • Femtoplankton (0.2 um) • Require host for replication (infection) • About1 order of magnitude more abundant than bacteria

16. Marine virus strategies: Lytic Chronic Lysogenic

17. A phage can either kill the cell (lysis), or transfer genetic material from a prior host (horizontal gene transfer) or from its own genome (accessory genes expression). The transferred genes can allow a cell to expand into different niches Similarly, small viral-like particles known as GTAs can transfer genes between organisms. Two scenarios could explain viral effects on cells. In the 'Red Queen' effect, the virus and cell are in an evolutionary 'arms race', in which they evolve resistance to each other until the virus ultimately kills the host cell. In the 'Cheshire Cat' hypothesis, the host moves from its diploid, non-mobile stage to a motile, haploid stage, thereby evading the virus.

18. In eutrophic, coastal environments • Producer biomass > Bacterial biomass • Metazoan grazers dominate the consumption of primary production • N and P lost from the system through fecal pellets (the fecal express!)

19. To summarize the relative importance of microbes in eutrophic and oligotrophic systems... Nutrients are locked up in the microbial loop in oligotrophic systems (where they play a greater role) Nutrients are exported by grazers in eutrophic systems (where they play a lesser role)

20. A revised view of the ‘microbial loop’: The ‘microbial web’ Class of newly discovered primary producers in open ocean < 5um • ‘Small’ production unavailable to larger grazing metazoans • Consumed by flagellate and ciliate grazers • Energy and material either recycled into microbial loop or passed to larger ‘exporters’ Large phytoplankton > 5um responsible for passing energy/material along to the ‘exporters’

21. The Microbial Web (Sherr and Sherr 1993)

22. When and where do microbial processes dominate the flux of carbon? Bacterial consumption of organic carbon exceeds carbon fixation NET HETEROTRPHY Primary production exceeds bacterial consumption NET AUTOTROPHY

23. Primary Production vs. Bacterial respiration Net Autotrophy Net Heterotrophy

24. Expect spatially discontinuous patterns... but there are also temporally discontinuous regions

25. Expect spatially discontinuous patterns... but there are also temporally discontinuous regions Estuaries and large river-dominated ecosystems have high fluxes of allocthonous organic materials to fuel high bacterial production. This can leads to one of the important symptoms of an unhealthy ecosystem: anoxia or hypoxia.