Microb Ecol (1994) 28:287-289

Controls of the Microbial Loop: Nutrient Limitations

MICROBIAL ECOLOGYInc. © 1994Springer-Verlag New York

Controls of the Microbial Loop: Nutrient Limitation and Enzyme Production, Location and Control C. Turley Plymouth Marine Laboratory, Citadel Hill, Plymouth PL1 2PB, UK

Abstract. A major controlling factor for bacterial growth is their ability to hydrolyze high molecular weight molecules too complex to be transported directly across the cell's membrane. The utility of such an extracellular enzyme hydrolysis system, location of the enzymes (free or attached), environmental controls of enzyme production, and implications of multiple hydrolysis-uptake systems are explored in relation to free-living oceanic bacteria and bacteria attached to rapidly sinking aggregates. Utilizable dissolved organic matter (UDOM), low molecular weight molecules that can cross the cell membrane using the active transport system, makes up only a small fraction of the total oceanic organic matter [4]. A major controlling force of bacterial growth is not only their ability to take up the UDOM at low concentrations but also to hydrolyze the more complex dissolved and particulate organic matter (POM) outside the cell membrane. Extracellular enzymes hydrolyze substrates too complex to be directly transported through the cell wall and can be bound to the cell membrane or in the periplasmic space (ectoenzymes), or dispersed in the water (free extracellular enzymes) [1]. Azam and Smith [1] developed "the enzyme pathway" hypothesis to explain the high carbon demand of free-living mesopelagic bacteria [3]. These investigators propose solubilization of the sinking POC pool by attached bacteria with a loose hydrolysis-uptake system, so that the DOM produced will supply the needs of free-living bacteria. They propose that free-living bacteria have cell-bound exohydrolases (POM and polymers are cut at the end producing dimers and monomers) resulting in tight coupling between enzyme production and substrate uptake, while bacteria attached to particles have free endohydrolases (POM is cut internally producing oligomers and polymers) resulting in a loose uptake system [1]. The relationship between UDOM concentration and uptake, control of ectoenzyme production, and POM concentration and hydrolysis in the aggregate will vary, with different biogeochemical consequences. Temperature and pressure may also play a role in enzyme inhibition [8] and with a high particle sinking speed could result in low levels of POC solubilization. Indeed, particles during the highest period of flux to 3,100 m in the Atlantic were rich in both POC and bacteria and had a low C:N ratio (6.5-7.0) indicating relatively undegraded material [9]. If aggregates do not escape the upper mixed layer before the UDOM is utilized and the ectoenzymes induced, then solubilization of the particle in the top 1,000-2,000


C. Tudey

m is likely. More slowly sinking particles are likely to contribute more to the carbon demand of mesopelagic bacteria while rapidly sinking ones escape significant solubilization. Indeed, relatively fresh aggregates are often found on the deep-sea bed [6]. Recent research indicates that attached and free-living bacteria may share no identical rRNA types, implying little or no interaction between the two populations [5]. Related species of the attached phenotypes degrade polmers by exoenzymes [5]. This supports the hypothesis that free-living and attached bacteria have different enzyme systems [1,7]. However, these distinct phenotypes may coexist since free-living bacteria can be incorporated into aggregates (e.g., by mucus web feeders). Chr6st [4] stated that there was no evidence that free extracellular enzymes are secreted by free-living bacteria, but recognized that they are often detected. However, "uncoupled hydrolysis" has been observed on aggregates [7]. Changes in the permeability of cells can lead to liberation of ectoenzymes and free extracellular enzymes. Release of ectoenzymes can vary with phases of growth and growth condition [4]. Could the aggregate environment enhance cell permeability or diffusion of the enzymes? Are intracellular enzymes released during cell lysis by viruses and during defecation during protozoan bacterivory on aggregates? What is the contribution of zooplankton to the particle enzyme pool after ingestion and repackaging by zooplankton? Wetzel [10] reminds us that "ecosystems are comprised of living cells and immobilized enzymes," that organisms that can reactivate these enzymes would be at a competitive advantage and that these enzymes can be transported in immobilized forms and reactivated at sites distant from the site of production. For example, do aggregates arriving on the sea bed carry immobilized enzymes produced in the surface waters and do the deep-sea bacteria reactivate these enzymes? Button [2] asks the important question of how many substrates are required for a cell to grow. This would obviously depend on the concentration of the substrates and the cell's ability to utilize them, which may vary within short time and space scales. Perhaps we can reverse the question and ask how many substrates can a bacteria utilize at one time? That is, what is the relation of genotype with phenotype and what factors control phenotypic expression? The degree of competition, specialization, or diversity within bacteria is likely to be influenced by the number of UDOM and POM substrates. Chrrst [4] found that aquatic bacteria are influenced by a range of environmental factors that determine the genetic expression of enzyme synthesis. Constant production of ectoenzymes is suppressed by catabolic repression, thus saving unnecessary expenditure of energy when UDOM is available. This control is exerted mainly at the level of transcription [4] and requires modulation of mRNA synthesis after induction or repression-derepression of an ectoenzyme, further energy saving being made by not producing unneeded transcripts. For a cell to make the greatest energetic gain from multiple enzyme production, it needs fight and separate control of induction and inhibition for each enzyme. The efficiency of carbon and energy transfer in the microbial loop and biogeochemistry of aquatic environments will depend on these genetic, metabolic, and environmental controls of ectoenzyme synthesis, activity, and regulation. Future research into the microbial loop may lie in the genetics of enzyme coding

Controls of the Microbial Loop


and the environmental feedback controlling the translational transcription of enzyme production within the cell. Acknowledgments. Karin Lochte, Phil Mackie and three reviewers gave thoughtful comments on the manuscript.

References 1. Azam F, Smith DC (1991) Bacterial influence on the variability in the ocean's biogeochemical state: a mechanistic view. In: Demers S (ed) Particle analysis in oceanography. (NATO ASI Series, vol G27) Springer Verlag, Berlin-Heidelberg, pp 213-236 2. Button DK (1994) The physical base of marine bacterial ecology. Microb Ecol 28:xxx-xxx 3. Cho BC, Azam F (1988) Major role of bacteria in biogeochemical fluxes in the ocean's interior. Nature 332:441443 4. Chrrst RJ (1991) Environmental control of the synthesis and activity of ectoenzymes. In: Chrrst RJ (ed) Microbial enzymes in aquatic environments. (Brock/Springer series in contemporary bioscience) Springer-Verlag, New York pp 29-59 5. DeLong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38(5):924-934 6. Gooday AJ, Turley CM (1990) Responses by benthic organisms to inputs of organic material to the ocean floor: a review. Phil Trans R Soc Lond A331:119-138 7. Smith DC, Simon AL, Alldredge AL, Azam F (1992) Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359:139-142 8. Turley CM (1994) The effect of pressure on leucine and thymidine incorporation by free-living bacteria and by bacteria attached to rapidly sinking particles. Deep-Sea Res 40:2193-2206 9. Turley CM, Mackie PJ (1994) Bacterial and cyanobacterial flux to the deep NE Atlantic on sedimenting particles. Deep-Sea Res (in press) 10. Wetzel RG (1991) Extracellular enzymatic interactions: storage, redistribution, and interspecific communication. In: Chrrst RJ (ed) Microbial enzymes in aquatic environments. (Brock/Springer series on contemporary bioscience) Springer-Verlag, New York pp 6-28

Controls of the microbial loop: Nutrient limitation and enzyme production, location and control.

A major controlling factor for bacterial growth is their ability to hydrolyze high molecular weight molecules too complex to be transported directly a...
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