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?

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

Traditional plate assays for counting bacteria indicated about 10 3 bacteria ml -1. Approximately equal (numerically) to phytoplankton Small size (100x smaller than phyto) suggested they were of minimal importance ecologically. 1950’s: Relatively large photosynthetic prokaryotes were recognized as important in Nitrogen cycling (e.g., Trichodesmium) HISTORY

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

Subsequent fluorometry of bacterial cells in 1980s showed an incredible under-estimation of bacterial concentrations in the sea... Not 10 3 ml -1, but ml -1 !! ~5 orders of magnitude more abundant than phytoplankton! Bacteria concentrations are relatively constant world-wide. HISTORY

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)

Where does the Dissolved Organic Carbon (DOC) required by bacteria come from? 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 Constant supply of dissolved organic substrates from phytoplankton

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’

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

Some bacteria derive energy to ‘fix’ CO 2 from reduced compounds such as hydrogen sulfide (H 2 S). Chemoautotrophy Where would we expect to find chemoautotrophic bacteria? Special cases...

Bacteria compete for substrates with phytoplankton. 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 Bacteria will out-compete phytoplankton for N and P, especially at low concentrations Uptake Rate Concentration Multiple transport systems for dissolved substrates enhances uptake over wide range of concentrations Bacterial advantages :

Decomposer biomass > Producer biomass Protozoans (flagellates and ciliates) graze heavily on bacterial production ‘Microbial Loop’ Phytoplankton Zooplankton Fish Bacteria (0.2-2 um) Flagellates (1-5 um) Ciliates (5-20 um) ‘Locks’ nutrients up in this recycling system Prevents losses to deep sea, but not much available for larger consumers. Why? In oligotrophic environments (mid-ocean gyres) (DOM )

The Microbial Loop (Azam et al. 1983)

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 Role of viruses in host metabolism may be more important than its role as an agent of mortality Marine viruses (discovered in late 1980s): Non-living, non-cellular particles Femtoplankton (0.2 um) Require host for replication (infection) About 1 order of magnitude more abundant than bacteria; their biomas is that of ~75,000,000 blue whales

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 gene expression). The transferred genes can allow a cell to expand into different niches. Small viral-like particles known as GTAs (Gene transfer agents) can also transfer genes between organisms. Two scenarios can explain viral effects. 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. In the 'Cheshire Cat' hypothesis, the host moves from a diploid, non-mobile stage to a motile, haploid stage, thereby evading the virus.

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!)

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)

A revision the ‘microbial loop’: The ‘microbial web’ Class of newly discovered primary producers in open ocean < 5um ‘Small’ production unavailable to larger grazing metazoans; is consumed by flagellates and ciliates 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’

The Microbial Web (Sherr and Sherr 1993)

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

Primary Production vs. Bacterial respiration Net Heterotrophy Net Autotrophy

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

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.

Marine virus strategies: Lytic Lysogenic Chronic

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? Special cases...