Journal of Experimental Marine Biology and Ecology 366 (2008) 99–103 Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe The microbial loop – 25 years later Tom Fenchel Marine Biological Laboratory, University of Copenhagen, Strandpromenaden 5, DK-3000 Helsingør, Denmark article info abstract Keywords: The background for and the subsequent impact on biological oceanography of the article Azam et al. [Azam, F., Functional types of microbes Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil, L.A., Thingstad, F. 1983. The ecological role of water-column Importance of names microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257-263.] is discussed. It is concluded that its influence in terms of Microbial loop stimulating further research and in changing the earlier paradigm of marine plankton food chains was to a large Recent discoveries extent due to the fact that the term “microbial loop” occurred there for the first time. The progress in understanding microbial biota and microbial interaction during the last 25 years will also be reviewed. © 2008 Elsevier B.V. All rights reserved. 1. Introduction organisms was substantial, meaning that microbes play a major role in the transformation of matter and energy in the plankton. More so- The term “microbial loop” was originally coined by Azam et al. phisticated methods for estimating in situ bacterial growth rates had also (1983), a paper on which both John and I were co-authors. The term has been developed (Hagström et al., 1979; Fuhrman and Azam, 1982). since then been a staple in the vocabulary of biological oceanography. Altogether it was recognised that bacteria play a substantial role The paper summarised and connected a variety of discoveries made comparable to that of the primary producers in terms of element cycling during the preceding decade by several marine biologists. Primarily it in the water column (Kirchman et al., 1982; Williams, 1981). was shown that the classic view of the structure of marine plankton It remained a problem to understand the fate of the apparently communities as presented by e.g., Steele (1976) was incomplete and substantial bacterial production. The bacterial density in the water too simplified. column usually remains relatively constant around 106 cells ml-1,but While the existence of tiny phototrophs, bacteria and heterotrophic other evidence indicated that bacteria were multiplying relatively fast protists in the marine water column had been recognised for a long time, with an average generation time of a day or less. Eventually it became most biological oceanographers believed that what really mattered in clear that bacterial density is mainly controlled by the grazing activity of the carbon cycle of the water column was only the production of large small protozoa and that in particular representatives of various phytoplankters, especially diatoms and dinoflagellates that served as taxonomic groups of flagellates are important. Such organisms occur food for zooplankton, mainly copepods, that again served as food for at densities of around 103 cells per ml seawater. It could also be small fish. concluded that their functional response to bacterial density and It had actually been recognised for some time that tiny photosyn- their capacity to ingest bacteria showed that ambient concentrations thetic plankton organisms (measuring 2-20 μm) also play a significant of bacteria were sufficient to sustain populations of these micro- role as primary producers (see Platt and Li, 1986). Bacteria in the water phagotrophs and also that grazing could explain the relatively constant column had also been studied and quantified using plate counts for density of bacteria in the water column. Under some circumstances the several decades (e.g., Zobell, 1946). It had also been noted that micro- population dynamics of bacteria and protozoa showed regular prey- scopic counts of bacteria exceeded plate counts by up to two orders of predator cycles that could be followed over longer time periods (Fenchel, magnitude, but it was generally believed that the bulk of microscopic 1982a,b,c). counts mainly included dead or metabolically inactive cells. Improve- The Azam et al. (1983) paper reviewed the available literature at the mentsintechniquesforcountingbacteria(Hobbie et al., 1977) combined time. It concluded that a substantial part of the primary production with the use of 14C-labelled substrates such as glucose and amino acids was lost to the environment in the form of dissolved organic matter as showed that a substantial part of the bacterial communities estimated had been shown by Fogg (1983) among others, and that dissolved from microscopic counts was actually metabolically active (Wright and organic matter was utilised by bacteria that were again consumed by Hobbie, 1965, Hobbie et al., 1972; Meyer-Reil, 1978), and Pomeroy (1974) protozoa, and finally that the protozoa could then enter the food chain had shown that the O2-uptake by the smallest size fraction of planktonic formed by larger creatures. Given a suitable graphical presentation, this new pathway in plankton dynamics forms a “loop” on the classic food chain (Fig. 1). The findings also showed that the characteristic E-mail address: [email protected]. time scale for the population dynamics and processes in the water 0022-0981/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2008.07.013 100 T. Fenchel / Journal of Experimental Marine Biology and Ecology 366 (2008) 99–103 Fig. 1. The microbial loop as described in Azam et al. (1983) (solid arrows) and with later additions (stippled arrows). DOC refers to dissolved organic matter. column in much shorter than hitherto recognised – bacteria as well as celerates mineralisation and thus regenerated production in nutrient their predators typically have generation times of less than a day. limited systems. During the years following the Azam et al. (1983) paper there was a spate of studies on the microbial loop treating a diversity of aspects 3. New players in the microbial loop related to it; for a long period these dominated biological oceano- graphy and many new discoveries were made. In the present mini- It early became apparent that there were more functional types of review I will list some of the highlights of research in the microbial loop organisms involved in the microbial loop than just phytoplankton, since the publication of Azam et al. (1983). Excellent in-depth reviews heterotrophic bacteria, and phagotrophic protists. In particular, it was of most aspects can be found in Kirchman (2000). Here I will only found that unicellular photosynthetic prokaryotes such as the mention some important developments since 1983 and especially ubiquitous Synechococcus play a substantial role as primary producers highlight aspects that I believe will be important in future research and and the more recently discovered minute prochlorophytes (Prochlor- that open up new questions. Finally I will discuss why especially Azam ophyton) were shown to dominate photosynthesis in oligotrophic et al. (1983) had such a large impact. oceanic waters (Chisholm, 1988, 1992; Cambell and Vaulot, 1993). The bacterium Roseobacter and relatives are so-called aerobe 2. Carbon cycling – link or sink? photoheterotrophs; they contain bacteriochlorophyll a like anaerobic phototrophic bacteria. Roseobacter cannot perform photosynthesis, A large part of the earlier effort was to document the quantitative role but it can generate ATP from light energy. Roseobacter often constitutes of the microbial loop and a variety of new methods were developed a large fraction of the bacterial plankton biota and it belongs to the mainly for estimating protozoan grazing rates and in situ growth rates relatively few quantitatively important plankton bacteria that are easy and growth efficiencies of bacteria (e.g., Kirchman et al., 1982; Fuhrman to isolate and grow on agar plates. The finding represents a novel and and Azam, 1982; Andersen and Fenchel, 1985; Sherr and Sherr, 1988; probably important energy input into the microbial loop (Kolber et al., Sherr et al., 1999; Caron and Goldman,1990; Del Giorgio and Cole, 1998) 2001). and these efforts also included modelling (Thingstad, 1992; Blackburn The most important new functional group is constituted by viruses. It et al., 1996). It became clear that the relative role of the microbial loop was found that viral particles occur at densities in seawater of about was not invariant over time and space. Rather the microbial loop dom- 109 ml-1 and their turnover rate could be estimated from their survival inates oligotrophic waters whereas as the classical plankton food chain rate in water in the absence of host cells (e.g., Proctor and Fuhrman, predominates under circumstances when there is a fresh supply of 1990; Bratbak et al.,1992; Thingstad et al.,1993). Viral attacks also play a mineral nutrients such as during the spring bloom in temperate waters role for eukaryotic algae. More recently, experimental studies have and in upwelling areas. This stands to reason in that competition for clarified a number of aspects concerning the role of virus. Almost all dissolved mineral nutrients favours small organisms and primary bacteria seem to have at least one host specific virus. Studies in the field production is then mainly based on mineral nutrients regenerated in and in laboratory systems have demonstrated the dynamics of virus- the water column (Chisholm, 1992; Kiørboe, 1993). host systems and the evolution of resistance and how virus may induce Another question that arose was the so called “link or sink” problem, lysis and thus recycles some dissolved organic matter from bacteria that is, to what extent the microbial loop represents a loss of fixed (Suttle, 1994; Suttle and Chan, 1994; Middelboe, 2000; Middelboe and carbon to the system or whether it primarily channels fixed carbon to Riemann, 2002, Middelboe and Jørgensen, 2006; Middelboe et al., 2001). higher levels of the food chain.