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Spatial Distribution of Viruses, Bacteria and Chlorophyll a in Neritic, Oceanic and Estuarine Environments

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Spatial Distribution of Viruses, Bacteria and Chlorophyll a in Neritic, Oceanic and Estuarine Environments MARINE ECOLOGY PROGRESS SERIES Vol. 92: 77-87, 1993 Published January 26 Mar. Ecol. Prog. Ser. I Spatial distribution of viruses, bacteria and chlorophyll a in neritic, oceanic and estuarine environments William P. Cochlan*, Johan Wikner **, Grieg F. Steward, David C. Smith, Farooq Azam Marine Biology Research Division, 0202, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California 92093-0202. USA ABSTRACT: The spatial distribution of viruses was investigated in the coastal and oceanic waters of the Southern California Bight, USA, and the brackish waters of the Gulf of Bothnia, Sweden, using the direct harvesting technique and transmission electron microscopy. The vertical and horizontal distribu- tions of viruses were examined in relation to bacterial abundance and chlorophyll a. Total virus abun- dances ranged from 0.3 to 52 X log1-l; higher concentrations of viruses were found in the upper 50 m of the water column and in coastal environments. Viruses with capsid diameters less than 60 nm dom- inated the virus community, were morphologically characterized as bacteriophages and were respon- sible for most of the observed spatial variability. Bacteria abundance alone explained 67 % of the spa- tial variability in virus numbers, thereby suggesting that bacteria constituted the major host organisms for viruses in these physically dlverse habitats. INTRODUCTION Fuhrman 1990) and numerous isolation of viruses with marine bacteria and algae as hosts (e.g. Cannon 1987, Viruses often numerically dominate the microbial Moebus 1987, Cottrell & Suttle 1991, Suttle et al. 1991, community in marine and freshwater environments Van Etten et al. 1991), strongly suggest that the major- with estimates of virus abundance generally ranging ity of viruses observed in seawater by transmission from 10' to 10" I-' (e.g. Bergh et al. 1989, Proctor & electron microscopy (TEM) are indigenous to the Fuhrman 1990, Hara et al. 1991, Wommack et al. 1992). aquatic environment, and constitute an active compo- The coupled dynamics of virus abundance with bacte- nent of the food web. ria and phytoplankton over a spring bloom period have Given the potential importance of viruses as agents been demonstrated, and marked increases in virus of mortality for phytoplankton and bacteria, and as numbers observed within an enclosed seawater sam- vectors of genetic information, there is a need for ple (Bersheirn et al. 1990, Bratbak et al. 1990). These knowledge of their spatial distribution in relation to the observations, together with the presence of phage- distribution of bacteria and phytoplankton. Quantita- infected bacteria in seawater samples (Proctor & tive distribution data may demonstrate the carrying capacity for viruses in different aquatic environments, Present adresses: and thereby indicate the likelihood for potential virus ' Hancock Institute for Marine Studies, University of proliferation. Few systematic studies of total virus dis- Southern California, Los Angeles, California, 90089-0373, USA tribution have been reported (Hara et al. 1991, ' ' Umea Marine Scientific Center. Box 3124, S-903 04. UmeA. Wommack et al. 1992) and only 1 with detailed depth Sweden profiles (Hara et al. 1991). Both studies were in bays 0 Inter-Research 1993 7 8 Mar. Ecol. Prog. Ser. 92: 77-87 and little is known about virus distribution in more were sampled in the Gulf of Bothnia off northern open coastal waters. Furthermore, it is not yet clear Sweden aboard the Swedish Coast Guard Vessel 'KBV how viral abundance relates to the biomass of bacteria 04' during August 1991: Bothnian Bay (Stn F9), and phytoplankton, although virus-to-bacteria ratios Bothnian Sea (Stn USSB), and a coastal station off the have been shown to vary by almost an order of magni- Norrby Archipelago (Stn NB1). Station locations are tude (e.g. Wommack et al. 1992). Based on the prevail- shown in Table 1. Seawater samples were collected ing perception that algae and bacteria are the major between 07:OO and 09:OO h, using l0 1 PVC Niskin or viral hosts, we would expect a correlation to emerge Hydro-Bios bottles (both equipped with silicon springs) with either of these parameters. There is also a paucity in California and Sweden, respectively. Samples were of information on the in situ distribution and spatial immediately transferred to acid-cleaned and rinsed, variation of viral size (Bergh et al. 1989, Bratbak et al. high-density polyethylene bottles. 1990, Wommack et al. 1992);information that could be Chlorophyll. Duplicate samples for chl a were col- relevant to the trophic fate of viruses. lected on Whatman GF/F filters and stored frozen in a Here we present direct counts of total virus abun- desiccator. Chl a was extracted in methanol overnight dance by TEM as a function of depth in the water col- and analyzed by in vitro fluorometry (Holm-Hansen & umn and distance from shore in coastal and oceanic Riemann 1978) using a Turner Designs Model 10 fluo- environments off southern California, USA (Southern rometer. Reported chl a values have been corrected for California Bight), and the brackish water environment phaeopigments determined after acidification. off northern Sweden (Guil ol Boiiiniaj. Vertical proiiies Bacteria abundance. Sampies for bactena counts of the size distribution of viruses at the different loca- were fixed with borate-buffered formalin (2 % final tions are also reported. The relationships of virus conc.) and stored at 4 "C in the dark until counted abundance to bacterial abundance and chlorophyll a (generally within 6 h of sampling aboard ship). (ch! a), and the irr.p!icatiocs for thcir hosts and the pop- Samples were eniimeraied by epifluorescence rnicros- ulation dynamics of marine viruses in natural marine copy following 10 min staining with 4',6-diamidino-2- systems are discussed. phenylindole (DAPI; Porter & Feig 1980), filtration on black, 0.2 pm Nuclepore filters and immediate mount- MATERIALS AND METHODS ing in parafin oil on glass slides. At least 200 cells or 20 fields were counted on each filter. We did not distin- Sampling. Two separate transects of stations were guish among the various types of procaryotes (e.g.het- sampled in the Southern California Bight aboard the erotrophic bacteria, coccoid cyanobacteria and pro- RV 'Robert Gordon Sproul'. A transect off Santa chlorophytes). Monica was sampled during September 1990 and 1991 Virus abundance. Samples (50 ml) were preserved (Stns 301, 303A, 304 & 305), and a transect off La Jolla with electron microscopy grade glutaraldehyde (2.5 % (Scripps Pier) and into the San Diego Trough (Stns T2, final conc.) and stored in sterile polypropylene centri- T5 & T8) was sampled in December 1991. Three sites fuge tubes in the dark at 4 "C. Harvesting of viruses was performed by ultracentrifugation directly onto Table 1. Description of stations sampled in the Southern TEM specimen grids in a procedure adapted from that California Bight and Gulf of Bothnia during 1990 and 1991 of Nomizu & Mizuike (1986). The grids (200 mesh Cu, coated with carbon-stabilized Formvar film; Pelcom Stn Maximum Location Distance from Ted Pella Inc.) were rendered hydrophilic by depth from shore high-voltage glow discharge (50 kV for 60 S) under (m) (km) vacuum; negatively charging the grid film prevents particle aggregation during drying (Hayat & Miller Southern California Bight 305 905 33" 45.12' N, 118" 55.09' W 46 1990). For each sample, 2 treated grids were placed 304 217 33" 54.18' N, 118" 38.26' W 18 into specially-constructed holders (details in Wells & 303A 55 33" 55.71' N,118" 31.92' W 7 Goldberg 1992) at the bottom of 13 m1 polyallomer cen- 301 16 33' 54.00' N,118" 26.50' W 0 9 trifuge tubes (Beckman). Subsamples (10 ml) were centrifuged (Beckman models L7, L8-M, L5-75B) using a swinging bucket rotor (SW41) at 41 000 rpm (288 000 X g) for 4 h at 25 "C. After centrifugation, the super- natant was carefully withdrawn and the grids stained Gulf of Bothnia with uranyl acetate (0.5% w/v) followed by multiple US5B 229 62" 35.20' N,19" 58 32' E 63 F9 129 62" 42.50' N,22" 04.00' E 33 rinses wlth 0.1 pm filtered glass-distilled water or NB l 25 63' 30.50' N, 19" 48.00' E 3 0.2 pm filtered Milli-Q@ water. It was calculated, using Stokes Law for the velocity of sedimentation, Cochlan et al.: Spatial distribution of viruses in three environments 79 that 55s particles (determined at 20 'C in distilled 5 different grid openings. Counts were made directly water) of 50 nm in diameter would sediment with from the electron microscope screen at 40000 to 100 '% efficiency under these conditions. To test parti- 82 000X magnification, whereas greater magnifica- cle recovery efficiency, we centrifuged a monodis- tions (100 000 to 400 000X) were used for photography persed (ultrasonicated) suspension of latex micro- and measurement of virus dimensions. Viral abun- spheres (87 nm diameter; Ernest F Fullman Inc.) and dance estimates were calculated taking into account compared these counts with those determined by the taper correction for non-parallel particle trajecto- counting (scanning electron microscopy) complete ries during centrifugation (Mathews & Buthala 1970). drops (n = 6) air-dried directly onto grids. Recovery ef- Statistics. Correlation analyses were conducted ficiency was 93 ? 0.2 % for the latex spheres under using the data from individual stations (complete these conditions. As an additional test of particle sedi- depth profiles) as well as combining the data (all sta- mentation efficiency, we found that a marine phage tions and depths) for a particular cruise. The correla- isolate (50 nm capsid size, non-tailed) was completely tion coefficient (r) of normally distributed data was removed from the supernatant after 2 h of centrifuga- calculated by the usual Pearson product moment tion, as determined by plaque assays of supernatent approach.
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