Inorganic nutrient limitation of oceanic bacterioplankton

Although it is commonly accepted that dissolved organic carbon (DOC) of algal origin limits bacterial growth in pelagic systems, there arc relatively few empirical studies documenting this effect. Depending on site and season, both organic and inorganic nutrients can limit the growth of freshwater bacteria. By contrast, inorganic nutrients have only recently been implicated as potentially growth-limiting for marine bacteria. At stations in the Gulf Stream, Sargasso, and Caribbean seas, we used a factorial experimental design to examine effects of inorganic (NH,, and PO,) and organic (glucose) nutrients on the uptake of thymidine and leucine and changes in bacterial abundance. Bacterial growth in seawater dilution cultures varied with station and treatment. Growth rates for the unamended controls (mean 2 SD = 0.11 +_ 0.02 d-l) were not significantly different among the stations or from the in situ rates. In the Caribbean Sea, additions of NH, and PO, resulted in a modest increase in growth rate (p = 0.20-0.35 d--l), whcrcas glucose, either alone or in combination with PO, and NH,, resulted in the largest increase (p = 0.500.55 d-l). By contrast, in the Gulf Stream and Sargasso Sea, the addition of glucose, either alone or in combination with NH,,, resulted in the smallest increase in growth rate (F = 0.2-0.4 d I), whereas the addition of PO.,, either alone or in combination with glucose and NH,, resulted in the largest increase (p = 0.55-0.60 d-l). Growth rates in the PO,,-amended seawalcr culture were 5-6-fold greater than the controls, suggesting that ambient concentrations of labile DOC were sufficient to sustain vigorous growth. We propose that PO, limitation or‘ bacterial growth may directly influence the accumulation of DOC in the surface layer and thus have a significant impact on carbon cycling in the sea. If bacterial growth were not constrained by inorganic nutrients, more DOC could be assimilated into bacterial biomass and subsequently transferred to protistan and metazoan grazers. At the third trophic step beyond bacteria, >90% of the DOC initially assimilated would be released as CO, and <5% would be transferred to mesozooplankton and hence converted into exportable biomass. Thus, when bacterial growth is P limited, the quantity of biogenic carbon (POC + DOC) exported to depth may be greater than would occur if DOC were first incorporated into bacterial biomass. The principal factors regulating bacterial growth and abundance are temperature, substrate supply, predation, and viral mortality (Caron 199 1; Ducklow and Carlson 1992; Shiah and Ducklow 1994~~; Fuhrman and Nobel 1995 and references cited therein). Surprisingly, however, the qualitative and quantitative relationships among these factors arc poorly understood. In temperate and tropical oceans, bacterial activities are normally regulated by temperature when water temperatures are low and by substrate supply, grazer predation, or viral mortality during the warmer periods (Hoch and Kirchman 1993; Shiah and Ducklow 1994b; Felip et al. 1996 and others). It has been inferred from the positive correlation between phytoplankton and bacterial biomass Acknowledgments This research was supported by National Science Foundation grants (OCE 83-00739, 83-14708, and 85-16214) to R.B.R. Grants Cram the Natural Sciences and Engineering Research Council of Canada (to R.B.R.) were instrumental in completion of this work. We gratefully acknowledge the help of the captain and crew of RV Cupe Hatteras, and thank D. Gustafson and K. Gloerson for outstanding technical assistance with sample collections and analysis. We thank H. Ducklow for use of his epifluorescent microscope and for many stimulating discussions about microbial ecology. K. Cracker, D. Deibel, and C. Parrish provided helpful comments on the manuscript. and production that phytoplankton exudates are the primary autochthonous source of organic substrates for bacterial growth (Cole et al. 1988). However, viral lysis of both bacteria and algae and the release of dissolved nutrients by protistan and metazoan grazers (originating from sloppy feeding, excretion, and the leaching and disintegration of fecal pellets) may also be significant mechanisms for the production of dissolved organic and inorganic nutrients (Jumars et al. 1989; Bratback et al. 1994). Although bacteria must assimilate organic carbon, they can use both inorganic and organic nitrogen and phosphorus and frequently account for a large fraction of PO, and NH, uptake in both freshwater and marine habitats (Currie et al. 1986; Currie 1990; Kirchman 1994). Studies in fresh water clearly show that bacteria can effectively compete with phytoplankton for these mineral nutrients (Currie and Kalff 1984a; Vadstein et al. 1988), however, comparable nutrient competition studies in marine systems are less common (Faust and Correll 1976; Suttle et al. 1990; Hoch and Kirchman 1995). Implicit in the apparent positive correlation between phytoplankton and bacterial biomass and production (Cole et al. 1988; White et al. 1991) is the assumption that bacterial growth in the sea is limited by the availability or quality of dissolved organic carbon (DOC). Studies in fresh water show that, depending on site and season, organic substrates,