Relation between presence‐absence of a visible nucleoid and metabolic activity in bacterioplankton cells

Abstract

We investigated the report of Zweifel and Hagstriim that only a portion of marine bacteria contain nucleoids --the DNA-containing regions of procaryotic cells-and that such bacteria correspond to the active or viable fraction of bacterioplankton.In Oregon coastal waters, 21-64% of bacteria had visible nucleoids; numbers of nucleoid-visible (NV) bacteria were greater than numbers of metabolically active bacteria, based on cells with active electron transport systems (ETS) and intact cell membranes. During log growth of a marine isolate, proportions of NV and ETS-active cells approached 100%. In stationary growth phase, the fraction of ETS-active cells decreased rapidly, while that of NV cells remained high for 7 d. When starved cells of the isolate were resupplied with nutrient (50 mg liter-l peptone), total cell number did not increase during the initial 6 h, but the proportion of NV cells increased from 27 to lOO%, and that of ETS-active cells from 6 to 75%. In an analogous experiment with a bacterioplankton assemblage, a similar trend was observed: the number of NV cells doubled during the initial 6 h prior to an increase in total cell counts. These results show that some bacteria without visible nucleoids are capable of becoming NV cells, and thus have DNA in a nucleoid region not detectable with the method used here. Enumeration of bacterioplanktonby staining with the fluorochromes acridine orange or 4',6-diamidino-2-phenylidole (DAPI) and then counting via epifluorescence microscopy is one of the most common methods used in aquatic microbiology. Zweifel and Hagstriim (1995) presented evidence that only a fraction of the cells counted with these methods appear to be living bacteria. They based this observation on the presence or absence of a nucleoid-a region packed with condensed DNA in the bacterial cell. The standard direct count method based on DAPI staining of aldehyde-preserved marine bacteria (Porter and Feig 1980) was shown to be nonspecific for DNA; a modification of the method resulted in efficient binding of DAPI to DNA and removal of most nonspecific DAPI staining of other cell components (Zweifel and Hagstrijm 1995). In seawater taken from the Baltic Sea, the North Sea, and the Mediterranean Sea, Zweifel and Hagstriim reported that from 2 to 32% of bacterioplankton appeared to contain nucleoids. They inferred from their results, which included laboratory culture experiments, that cells with nucleoids corresponded to the portion of the bacterial assemblage that is active or viable and that cells without nucleoids were "ghost" cells that did not contain DNA and were therefore incapable of growth.Acknowledgments

Dormancy contributes to the maintenance of microbial diversity

“…A sometimes-large but variable fraction (20-80%) of the bacteria recovered from environmental samples appear to be metabolically inactive (14). Although some of these cells are dead or moribund, other populations can be resuscitated with resource supplements (15). Despite evidence that dormancy is widespread, we have little theoretical expectation as to how it influences the structure of natural, complex microbial communities.…”

Factors controlling benthic metabolism during low tide along a granulometric gradient in an intertidal bay (Roscoff Aber Bay, France)

“…Thus, estimation of the bacterial abundance would be overestimated with DAPI counts (i.e. only a small fraction of the bacterial community is active, Zweifel & Hagström 1995, Choi et al 1996, rather than overestimation by counting bacteria plus ciliates. The bacterial respiration estimation proposed in this study was thus based on bacterial biomass only and would represent the contribution of bacteria only.…”

Diel periodicity of bacterioplankton in the euphotic zone of the subtropical Atlantic Ocean

“…This decline in bacterial abundance is accompanied by only a 2-to 3-fold decline in the concentration of dissolved organic carbon (DOC) from the surface waters to the deep ocean. Even if a considerable fraction of the bacterioplankton in the upper mixed layer is inactive , Choi et al 1996, Heissenberger et al 1996, Karner & Fuhrman 1997, Vosjan & Noort 1998, the ratio between bacterioplankton production and DOC concentration is lower in the deep ocean as compared to the surface waters. This implies low turnover rates of DOC in the deep ocean and lower loss rates for the deep water bacterioplankton.…”