1
Setting the Scene

Intention: This chapter provides a basis for the biological and biogeochemical knowledge needed for the rest of this book.

To make the subsequent chapters accessible to readers with different backgrounds, this introductory chapter has three parts: (1) an introduction to the world's oceans and the role of microbes in its biogeochemical processes; (2) a brief introduction to the competitive and defensive traits of main functional groups of marine micro-organisms; (3) a short review of how the combination of new methodologies and new concepts has shaped contemporary ideas about the functioning of the marine microbial food web (MMFW).

Box 1.1 Important concepts of Chapter 1

Important concepts:

• Marine microbial food web (MMFW). The part of the marine food web consisting of unicellular organisms and their viruses. Only the pelagic part of the marine food web is discussed here.
• Photic zone. The upper layer where light is sufficient for photosynthesis to occur. With a maximum depth of 200?m, and 20?m a more typical value in coastal waters, the photic zone is a thin 'skin' on top of a vast ocean interior (an average depth of 3688?m).
• Pycnocline. A layer in the ocean with a steep gradient in water density. This can be either a thermocline where the density change is caused by a warm upper layer floating on top of cold deep-water or a halocline where low salinity water floats on top of high-salinity deep-water. Pycnoclines work as mixing barriers, reducing water exchange between the two layers.
• Mixing depth. There is a mixed layer extending from the surface to the mixing depth. It is not a mixing occurring at the mixing depth.
• Compensation depth and critical depth. Compensation depth is where phytoplankton's gross photosynthesis and respiration are equal. Critical depth is where gross photosynthesis and respiration, when integrated over the water column above, equals.
• Limiting nutrient. In the photic zone, photosynthetic production of biomass is linked to the consumption of elements other than carbon, needed to produce cells. When one of these is depleted, it limits the growth of phytoplankton and is referred to as the limiting nutrient. In some contexts, the element (e.g., N) is more important than its chemical forms (e.g., ammonium, nitrate, or urea), hence, we will use the term 'limiting element'. In the ocean, the growth-limiting element is typically N, but in some regions can also be P or Fe.
• Nutricline. A layer in the ocean where the concentrations of limiting nutrient increases from the photic zone to the aphotic zone.
• Upwelling. When nutrient-rich deep-water is transported to the photic zone.
• Redfield ratio. The C:N:P molar ratio of 106 : 16 : 1 which is the average stoichiometry of particles in the upper ocean.
• Photic zone nutrient content. The total amount of limiting element available in the photic zone for sharing among all biologically active forms. This limits the total biomass that can be formed. In addition to the amount of the element incorporated into the organisms, it includes the summed concentration of the free forms of limiting nutrient (e.g., ammonium?+?nitrate?+?urea).
• Import, regenerated and export production. Imported production is the part of photic zone primary production based on imported limiting elements (also called new production). The other part, regenerated production, is based on limiting nutrients recycled within the photic zone. Export production is the amount exported to the photic zone.
• Ocean conveyor belt. A large-scale ocean circulation transporting deep-water from the North Atlantic to the North Pacific and returning to the North Atlantic as surface currents.
• Ocean carbon sequestration. The process whereby carbon is from the atmosphere and transported to the ocean's interior.
• Biological pumps. The biological mechanisms involved in ocean carbon sequestration.

1.1 The Physical and Chemical Environment of the MMFW

About two-thirds of the earth's surface is covered by ocean. Because of the conditions for life in water, primary producers in this biotope are micro-organisms. As a result, about 50% of the world's primary production occurs in the MMFW (Mattei and Scardi, 2021), not only feeding the world's large fisheries but also leading to an ocean sequestration of about 30% of the CO2 emissions from our burning of fossil fuels (Gruber et al., 2019).

The solar energy absorbed by the earth is dissipated through two systems: physical and biological. Most of this energy is dissipated through the physical systems consisting of the circulations in the atmospheric and the ocean and the associated hydrological cycle. A small part of the energy (about 1-2% (Thompson et al., 2024)) enters photosynthesis where the organic material synthesized fuels the food webs that drive cycles of biologically active elements and oxidate the organic-C back to CO2.

The physical dissipation system is a main driver of the biological systems. The key role of the hydrological cycle for terrestrial systems is demonstrated by the earth's large desert regions. In the ocean, where water is not a limiting factor, a main coupling comes from how dominant wind systems affect water circulation and the availability of growth-limiting elements, primarily N, P and Fe in the photic zone. When warm air rises along equator, it is replaced by air from higher latitudes. Deflected by the Coriolis force, this sets up an east-to-west wind along the equator. When this warm air is cooled in the upper atmosphere, it sinks back down at around 30° latitude, now forming a dominant west-to-east wind. In the Atlantic, these winds are known as the trade-winds because European traders used them to sail via West Africa to America along the Equator, returning at more northernly latitudes in the Atlantic. Where these dominant winds blow off the continents, surface water is transported away from the coast and replaced by nutrient-rich deep-water. The resulting combination of light and nutrients generates huge phytoplankton blooms, particularly visible off western Africa and Peru (Figure 1.1).

The El Niño phenomenon is when, in the Pacific, the equatorial east-west current changes the direction. The upwelling along the Peruvian coast then shifts to downwelling, nutrient-poor surface waters, reduced primary production, and a food chain that cannot support the plankton feeding anchovies.

North and south of the equator, there are large chlorophyll-poor regions (Figure 1.1) called the oceanic gyres. These are caused by a permanent thermocline that prevents mixing between the nutrient-poor photic zone and the nutrient-containing deep-water. The result is a permanently low photic zone nutrient content and therefore little biomass. The photic zone nutrient content does not only regulate how much biomass can be formed but is also an important driver for the structure of the MMFW: in the oligotrophic gyres, it is dominated by small (0.5-1.5?µm) pico-phytoplankton (Figure 1.2), while upwelling areas are typically dominated by large-celled (1-2 orders of magnitude larger, typically diatoms) species. The background for this can be understood from a simple steady-state argument: When the nutrient exchange between the photic and aphotic zones is in a steady state, import and export from the photic zone must be balanced. When the import is low, as in the gyres, the steady-state structure of the photic zone MMFW must produce little export. Sinking rates increase rapidly with size (as r2 for a spherical particle). A food web dominated by free-living picoplankton will therefore produce much less export than one dominated by large diatoms ballasted with a heavy silicate frustule.

Figure 1.1 Global distribution of chlorophyll. Yearly average. From Global Chlorophyll (nasa.gov).

Source: Figure from NASA/SeaWiFS Project.

Figure 1.2 Traditional size-class divisions of plankton (logarithmic scale).

The vertical export of organic matter is an important biogeochemical function of the photic zone food web. It transports carbon, fixed by photosynthesis in the photic zone, to the ocean's interior (Figure 1.3). Most of this is oxidized to CO2 in deep-waters, but the carbon will not be exposed to exchange with the atmosphere until the deep-water is returned to the surface by ocean circulation. The average age of dissolved organic carbon (DOC) as determined from the content of the radioactive 14C isotope is 4000-6000?years (Druffel et al., 2016). This has traditionally been taken as evidence for recalcitrance of the material accumulating. An alternative hypothesis is that it is not the chemical nature, but the low concentration of individual components that limits the degradation rate (Arrieta et al., 2015). The two mechanisms are not mutually exclusive and may both contribute to the high observed age.

Central in this process is the ocean's conveyor...