It has been known for many years that filtrates from axenic algal cultures may be enriched with organic compounds. These materials, including simple amino acids and peptides, sugars, polyalcohols, and occasionally vitamins, enzymes, and toxins, are usually lumped under the term "extracellular products" (Fogg, 1966). Studies using natural populations of phytoplankton have shown that extracellular products are not mere laboratory artifacts, and that, depending upon environmental conditions, they account for 1-20% of the total photoassimilated carbon (Hellebust, 1965;Nalewajko, 1966; Samuel, Shad and Fogg, 1971;Thomas, 1971).The potential significance of extracellular organic material in marine food chains is extremely interesting. Many authors (Fogg, 1966;Brock, 1966;Alexander, 1971 ; Whittaker and Feeney, 1971) have suggested that these products may play an important role in marine food chains, especially as potential nutrients for bacteria. However, to our knowledge, there is no direct evidence that this is so although the ability of bacteria to grow in algal cultures (Vela and Guerra, 1966;Berland, Bianchi and Maestrini, 1969) might be interpreted to support such conclusions.If, in fact, algal extracellular products are important contributors to bacterial food chains, it would seem possible to construct an aquatic counterpart of the wellknown "rhizosphere" of terrestrial ecosystems (Rovira, 1965). A zone may exist, extending outward from an algal cell or colony for an undefined distance, in which bacterial growth is stimulated by extracellular products of the alga. For purposes of discussion in this paper, we will term this region the "phycosphere."Motile bacteria commonly exhibit chemotaxis to concentration gradients of organic material (Weibull, 1960;Adler, 1969). The ecology of chemotaxis by organotrophic bacteria has not been well studied, but highly species-specific responses to certain carbohydrates, amino acids, and nucleotide bases have been observed (Fogel, Chet and Mitchell, 1971), and certain predatory microorganisms have been shown to be chemotactic to their prey (Chet, Fogel and Mitchell, 1971).
Two marine bacterial isolates differ considerably in their uptake rates of extracellular products produced by the alga Skeletonema costatum: 0.4 x 10WR pg 0 cell-l hr-l for spirillum 7697; 16 x lo-' ,ug C cell-l hr-l for pscudomonad HNY. These disparate uptake rates are used to interpret the growth patterns of the bacteria in the presence of the alga on a seawater inorganic enrichment medium. Pseudomonad HNY grows well with the alga in both batch and continuous culture, in the latter attaining a steady state population two orders of magnitude greater than achieved in the absence of the alga, Spirillum 7697, however, grows poorly in the presence of growing algal cells and appears to be inhibited to some cxtcnt under such conditions.Such observations suggest that dominant bacterial populations associated with algal blooms arc a result of both stimulation and inhibition mediated by the release of extracellular products.
The uptake of 14C-labeled extracellular products from Skeletonema costatum by native bacterial populations was analyzed during a bloom of this alga in the Trondheimsfiord, Norway. Data in agreement with the linear predictions of a mixed-substrate kinetic model were obtained on each of 10 separate occasions. Changes in the kinetic parameters indicated that a 4-fold increase in bacterial activity was enough to prevent a large accumulation of dissolved extracellular products. Transient inhibition of bacterial activity occurred during the late exponential phase of the algal bloom. Labeled extracellular products from Chaetoceros affinis were not utilized in a manner that could be analyzed according to the kinetic model. The data indicate that the bloom of S. costatum stimulated the activity of a specific bacterial flora which established a dynamic equilibrium between the release and consumption in situ of extracellular products,
Equations based on the kinetic model for estimating heterotrophic potential are derived which permit a linear kinetic analysis of the utilization of algal extracellular products by bacteria. Laboratory studies with a specific algal-bacterial system suggest that the analysis will show changes in heterotrophic population size and in concentrations of extracellular products. Deviations from linear predictions of the model may also reveal aspects of the degree of specificity of algal-bacterial interactions mediated by extracellular products. Application of the mixed substrate model may permit the detection and qualitative evaluation of the ecological significance of a phycosphere effect generated by algal blooms.
Kinetic analyses were made of the utilization of '"C-labeled algal extracellular products (EP) by bacterial populations in continuous algal cultures containing steady state Skeletonema costatum or Dunaliella tertiolecta. The development of bacteria adapted to the respective algal species was revealed by gradual evolution of a common X-intercept for net EP uptake and respiration lines from initially disparate estimates. When the adapted populations were given labeled EP prepared from other algal species, linear kinetics were retained but the X-intercepts for net uptake and respiration failed to coincide. Bacterial response to a given algal EP pool does not necessarily preclude enzyme-mediated utilization of organic substrates from other species. Rapid utilization of algal EP appears to be a consequence of bacterial adaptation to existence under dilute nutrient conditions rather than a response to a specific alga. Prolonged exposure to a single alga may favor the development of bacterial populations in which metabolism is limited by enzyme-mediated transport of the compounds available in its EP pool, but this phenomenon is less significant ecologically than the general stimulation of bacterial activity effected by the increased supply of these compounds.
Kinetic analyses indicate that members of natural bacterial populations from 2 marine environments near Woods Hole, MA, possess enzyme-mediated transport systems which permit utilization of(14)C-labeled extracellular organic C ((14)C-EOC) prepared from the algae,Skeletonema costatum, Thalassiosira pseudonana, andDunaliella tertiolecta, and supplied over a concentration range of 15-150μC·liter(-1). It is shown that previous exposure of the bacteria to the EOC from these algae cannot explain the linear kinetic patterns obtained. Therefore, the ability to utilize algal EOC at low concentrations is a general feature of metabolically active bacterial populations. Further, as the native bacteria do not restrict this ability to a specific EOC pool, the results are consistent with the hypothesis that bacteria adapted to low nutrient environments possess uptake systems of high substrate affinity and low substrate specificity. Elevation of substrate levels with as little as 10 mg·1(-1) peptone is shown to favor development of a bacterial population that lacks these adaptations. Standard enrichment techniques typically result in the isolation of bacteria that are poor models for evaluating the ecology of native microbiota.
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