The purpose of this section is to comment on some aspects of the fate of photosynthetic products at the local and global level. The profound impact that they exert on carbon cycling in plankton-based aquatic systems is also addressed. The preceding sections show a wide variation in the eventual allocation of the carbon fixed in photosynthesis. Well corroborated in the literature, the range extends from some 92% to 95% investment in new biomass (Talling, 1957c; de Amezaga et al., 1973; Knoechel and Kalff, 1978; Geider and Osborne, 1992) to disparately low (Talling, 1966; Pollingher and Berman, 1977; Peterson, 1978; Hecky and Fee, 1981). Zero net gains in biomass relative to photosynthesis (i.e. carbon fixation is balanced or exceeded by net losses: Reynolds et al., 1985) are observable when plankter growth is resisted by the total exhaustion of one or other of the essential nutrients. The relatively stable biomass of low-latitude oceanic phytoplankton, in spite of positive carbon-fixation rates (Karl et al., 2002), conforms to the latter diagnosis. The general pattern is that the coupling of net growth to photosynthesis is closest in well mixed, light-limited and nutrient-replete (but possibly carbon-deficient) water columns and weakest under conditions characterised either by stratification, or light saturation to a substantial depth, or extreme nutrient limitations, or any combination of these.
That there should be a gap between the amounts of carbon fixed and those eventually constituting new biomass is not in itself surprising, neither is the relative magnitude of the difference. It was once supposed that the shortfall was explicable in terms of mortalities of producer biomass, chiefly to settlement and to consumers and pathogens (Jassby and Goldman, 1974a). Estimating loss rate of biomass was not then well-advanced but the magnitude of biomass losses necessary to explain productive shortfalls of this order is, on purely intuitive grounds, unrealistically large. It was another perceptive analysis (Forsberg, 1985) that pointed out that, in study after study, the alleged loss of biomass was so close to the measured photosyn-thetic gain that perhaps the 'lost biomass' had never been formed in the first place. Instead, the losses of fixed carbon are predominantly physiological (for instance, through enhanced respiration), as had indeed been suggested by both Talling (1984) and Tilzer (1984).
The fate and allocation of what, to the pho-tosynthetic microorganism, is excess, unassimil-able and mainly unstorable photosynthate, has taken a little longer to diagnose. Certainly, a proportion is respired directly, or is fully pho-torespired to carbon dioxide and water. It had already been clear for over a decade, however, that a proportion is excreted as DOC, especially when cells are stressed by high insolation or depleted nutrititive resource fluxes (Fogg, 1971; Sharp, 1977). The circumstances of gly-colate excretion, in particular, had been diagnosed (Fogg, 1977), well before the circumstances of its regulated production through the accelerated oxygenase activity of the RUBISCO enzyme (see Section 3.2.3) and its beneficial role in protecting against photooxidative stress had been elucidated (Geider and MacIntyre, 2002). Many other organic compounds are now known to be released by algae into the water, often in solution but not necessarily all to do with metabolic homeostasis. They include monosaccharides, carbohydrate polymers, carboxylic acid and amino acids (Sorokin, 1999; Grover and Chrzanowski, 2000; Sondergaard et al., 2000).
Though they may be unusable and unwanted by the primary producers, at least in the immediate short term, these organic solutes provide a ready and exploitable resource to pelagic bacteria (Larsson and Hagstrom, 1979; Cole, 1982; Cole et al., 1982; Sell and Overbeck, 1992). The existence of bacteria in the plankton, both free-living and attached to small mineral and detri-tal particles in suspension, has for long been appreciated but, for many years, their role in doing much more than recycling organic detritus and liberating inorganic nutrients was scarcely appreciated. Interest in the ability of bacteria to assimilate the organic excretory products of pho-toautotrophs increased rapidly with the realisation that a large part of the flux of photosyn-thetically fixed carbon is passed to the food web through a reservoir of DOC rather than through the direct phagotrophic activity of metazoans feeding on intact algal cells (Williams, 1970, 1981; Pomeroy, 1974). It soon emerged that the chain of consumption of bacterial carbon - normally by phagotrophic nanoflagellates, then successively ciliates, crustacea and plantivorous fish - resulted in the transfer of carbon to the higher trophic levels. This alternative to the more traditional view of the pelagic alga ^ zooplankton ^ fish food chain soon became known as the 'microbial loop' (Azam et al., 1983). Indeed, it now seems that the 'loop' is often the only viable means by which diffusely produced organic carbon can be exploited efficiently by the fauna of resource-constrained pelagic systems. It is better referred to as the 'microbial food web' (Sherr and Sherr, 1988) or, perhaps, as the 'oligotrophic food web'. Its short-cutting by direct herbivory is then to be seen to be the luxurious exception, possible only when a threshold of relative abundance of nutrient resources is surpassed, sufficient to sustain a 'eutrophic food web' (Reynolds, 2001a) (see also Section 8.2.4).
For the present discussion, it is the mechanisms and pathways of phototrophically generated carbon that are of first interest. Progress has been hampered somewhat by an insufficiency of information about the identities of the main bacterial players and their main organic substrates. Knowing which 'bacteria' use what sources of 'DOC' sources is essential to the ecological interpretation of the behaviour of pelagic systems. Until quite recently, the identification of bacteria relied upon shape recognition, stain reaction and substrate assay. Now, microbiology is adopting powerful new methods for the isolation of nucleic acids (DNA and especially the 16S or 23S ribosomal RNA), their amplification through polymerase chain reaction (PCR) and their matching to primers specific to particular bacterial taxa. The approach is similar for both marine and freshwater bacterioplankton (good examples of each are given by Riemann and Winding, 2001; Gattuso et al., 2002). Methods of enumeration have advanced to routine automated counts by flow cytometry. The use of highly fluorescent nucleic acid stains makes for rapid and easy cyto-metric determination of microbe abundance and size distribution in simple bench-top apparatus (Gasol and del Giorgio, 2000). In consequence, the knowledge of the composition, abundance and dynamics of planktic microorganisms is now developing rapidly.
In both lakes and the seas, the free-living heterotrophic bacteria occur in the picoplanktic size range (0.2-2 |im; <4 |im3), which they share with the photoautotrophic synechococcoids and eukaryote picophytoplankton (in lakes) and coc-coid prochlorophytes (in the open ocean). Other key participants in the oceanic microbial food webs (viruses, protists) are also prominently represented in those of lakes. These structural similarities between marine and freshwater micro-bial communuties suggest that they both have
Table 3.4 Typical (upper) densities of bacterioplankton in lakes and seas and daily production rates.
Standing population Standing biomass Production (x I0-6mL-1) (mgCm-3) (mgCm-3d-1)
2-5 90-500 40-150
Deep (>800 m) tropical oceanic waters Surface tropical oceans Oligotrophic lakes Antarctic waters (summer) Temperate ocean Mesotrophic lakes Inshore waters, estuaries Oceanic coastal upwellings Eutrophic lakes Hypertrophic lakes, polluted lagoons
Source: Based on Sorokin, 1998.
ancient and, possibly, common origins. The typical cell concentrations present in either broadly fit within 2 orders of magnitude (105-107 mL-1), although pronounced seasonal variation is often detectable, depending upon temperature, the abundance of organic substrate and the intensity of bacterivorous grazing. It is clear that numbers generally reflect the trophic state and they are responsive to enhanced primary-producer activity (Nakano et al., 1998), especially in the wake of phytoplankton 'bloom' periods (Coveney and Wetzel, 1995; Sorokin, 1999; Ducklow et al, 2002) but there is no constant proportionality. Indeed, relative to algal biomass, bacterial numbers (104-1076 mL-1: Vadstein et al., 1993; Sorokin, 1999) (see also Table 3.4) diminish with higher nutrient availability (Weisse and MacIsaac, 2000). Using relationships resolved by Lee and Fuhrman (1987) for marine bacterioplankton, heterotrophs and photoautotrophs may each account for (roundly) up to 0.1 mg C L-1 of the phytoplankton biomass of substantially oligotrophic systems. Here, bacterial activity may exceed that of algae (Biddanda et al., 2001) and, thus, make relatively the greatest contribution to organic-matter cycling. In another recent study of the carbon flux through the oligotrophic microbial community of the Bay of Biscay ([chla] < 0.7 mg m-3), Gonzalez et al. (2003) found that a gross primary production (GPP) rate of ~230mgCm-2 d-1 was considerably exceeded by bacterial respiration rate (1740 mg C m-2 d-1) but with little change either to the bacterial abundance or to the DOC pool (indicating almost no biomass accumulation and complete pelagic cycling of CO2). Significantly, an upwelling event, with a consequent pulse of nitrogen, stimulated GPP (to over 900 mg C m-2 d-1) and to the net recruitment through growth of phytoplankton, leading to an enhanced biomass of larger species 'exportable' as food or in the sedimentary flux. The bacterial biomass decreased, relatively and absolutely, presumably in response to the rerouting of photo-synthetic carbon. Where conditions are typically more eutrophic, supporting biomasses of >2.5 mg algal C L-1, bacterial mass may scarcely exceed 0.5 mg C L-1.
The species structure of the bacterioplank-ton is highly varied and, collectively, includes species capable of oxidising substrates as varied as carbohydrates, various hydrocarbons, proteins and lipids (Perry, 2002). Presumably, the numbers of the particular types fluctuate in response to substrate supply and to grazing: distinct species 'successions', in time and in space, have been demonstrated as the community composition responds to the dissipation of substrate pulses moving through linear mainstem reservoirs (see especially Simek et al., 1999). Interestingly, however, the clearest trends in species composition seem to respond - like the phytoplankton itself -to the availability of inorganic nutrients. Olig-otrophic and mesotrophic assemblages in lakes (e.g. Simek et al., 1999; Lindstrom, 2000; Riemann and Winding, 2001; Gattuso et al., 2002) and in the sea (Fuhrman et al., 2002; Cavicchioli et al., 2003; Kuuppo et al., 2003; Massana and Jurgens, 2003) are commonly dominated by species of the Cytophaga-Flavobacterium group and/or various genera of a- and y-proteobacteria. It also seems likely that these are the main groups of bacteria colonising particulate organic detritus (Riemann and Winding, 2001), some of which anyway decomposes and disintegrates rapidly (Legendre and Rivkin, 2002a). The detailed studies of Cavicchioli et al. (2003) on the dynamics of the proteobacterium Sphingopyxis reveal the relevant properties of an oligotrophic het-erotroph. Besides its small size and high surface-to-volume ratio, this obligately aerobic bacterium has a high affinity for nutrient uptake. Population growth rates are sensitive to availability of substrates (which include malate, acetate and amino acids) and to the supply of inorganic ions.
It is clear from this that, although plank-tic photoautotrophs and heterotrophs have quite independent carbon sources, they nevertheless have to compete for common sources of limiting inorganic nutrients. Moreover, it is likely that the bacteria are superior in this respect (Gurung and Urabe, 1999). Potentially, a mutualism develops between nutrient-deficient autotrophs and carbon-deficient heterotrophs. The elegant experiments of Gurung et al. (1999) on the plankton of the oligotrophic Biwa-Ko, Japan, illustrate how this balance might be maintained. Under low light, photosynthesis is low and bacterial growth is constrained by low organic carbon release. Increasing the light to nutrient-limited phytoplankton stimulates the supply of extracellular organic carbon and the growth of het-erotrophs (and of their phagotrophic consumers). Raising the resources available to the photoau-totrophs, however, interferes with the organic carbon release to the increasing limitation of het-erotroph production. With increased nutrients, the producers retain proportionately more photo-synthate and invest it in the production of their own biomass.
In reality, planktic systems are rather more complex than this simple model might indicate. One major distorting factor is the complicating and paradoxical role played by other, usually much more abundant, sources of dissolved organic matter in pelagic environments. In particular, dissolved humic matter (DHM) is often, by far, the major component of the DOC content of natural waters. Indeed, in the open ocean, where there is a fairly invariable base concentration of ~1 mg L-1 of DOC (Williams, 1975; Sug-imura and Suzuki, 1988), in lakes where concentrations typically fall in the range, 1-10 mgCL-1 (Thomas, 1997), and in brown, humic waters draining swamps and peatlands and in which humic matter accounts for 100-500 mg C L-1 (Gjessing, 1970; Freeman et al., 2001), DHM may represent some 50-90% of all the organic carbon (including organisms) in the pelagic (Wetzel, 1995; Thomas, 1997). The supposed origin of this varied material - decomposing terrestrial plant matter - is plainly self-evident in lake catchments, although neither the flux to the sea nor its persistence in the ocean has been fully verified.
DHM has the reputation of resistance, or recalcitrance, to degradation by bacteria. Humic material appears in water as substances, mainly phytogenic polymers, of relatively high molecular weight and complexed with various organic groups, which include acetates, formates, oxalates and labile amino acids. By the time they leach into water some decomposition has already taken place. The diversity of humic materials, already large, is increased further (Wer-shaw, 2000): to make any kind of general assessment of the availability of DHM to pelagic bacteria is still difficult, awaiting more research. However, Tranvik's (1998) thorough evaluation of the bacterial degradation of DOM in humic waters presents some well-considered analysis. Many humic compounds are amenable to bacterial decomposition but, generally, the yield of energy to bacteria is rather poorer than non-humic DOM. Most is relatively refractory but the resultant pools are not unimportant as bacterial substrates, even though they turn over slowly. The rate of oxidation is influenced by the availability of other nutrients, their tendency to flocculate and their exposure to sunlight and photochemical cleavage. This last turns out to be crucial, as the photodegradation of organic macro-molecules to more labile and more assimilable products is now known to occur under strong visible and ultraviolet irradiance (Bertilsson and Tranvik, 1998, 2000; Obernosterer et al., 1999; Ziegler and Benner, 2000). As a result, many relatively simple, low-molecular-weight organic radicals may become available to microbes and may not necessarily be readily distinguishable from the DOM released by photoautotrophs (Tranvik and Bertilsson, 2001).
The emphasis may still be on the restricted nature of the photodegradation and its confinement to surface layers, for the general impression of slow decomposition of humic matter endures. It is likely that it is only in shallow-water systems where allochthonous inputs of DOM might sustain the predominantly hetertrophic activity that the relative abundance of organic carbon would lead us to expect. Elsewhere, it is mainly the non-humic, autochthonously produced DOC that seems likely to underpin heterotroph activity.
This last deduction fits most comfortably with the previously noted general coupling between bacterial mass and primary production: the supposition that, on average, around half the primary production of the oligotrophic pelagic passes through the DOC reservoir requires that this must also be the more dynamic source of carbon and this supports the more active part of bacterial respiration (Cole et al., 1988; Ducklow, 2000). Of course, the relationship is approximate, it is difficult to predict precisely and is plainly subject to breakage. High rates of bacterivory, for instance, would cause one such mechanism. However, bacterial growth can become nutrient limited in very oligotrophic waters, to the extent of positive DOC accumulation (Williams, 1995; Obernosterer et al., 2003), just as easily as it can be substrate limited in (say) nutrient-rich estuaries (Murrel, 2003). In this context, it is especially interesting to note the reports of oceanic microbiologists referring to atomic C : N ratios in pelagic bacterial biomass of 4.5 to 7.1 (Kirch-man, 1990) are interpreted as being indicative more of carbon than of nitrogen limitation of bacterial growth (Goldman and Dennett, 2000). Clearly, the relatively abundant forms of DOC in the oceanic pools often fail to satisfy the requirements of the most abundant planktic het-erotrophs, which must therefore rely predominantly on the excretion of phototrophs, much as the Gurung et al. (1999) model suggests. Equally clearly, it is a relationship of high resilience (Laws, 2003).
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