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Importance of Heterotrophic Bacterial Assimilation of Ammonium and Nitrate in the Barents Sea During Summer

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Importance of Heterotrophic Bacterial Assimilation of Ammonium and Nitrate in the Barents Sea During Summer J O U R N A L O F MARINE SYSTEMS ELSEVIER Journal of Marine Systems 38 (2002) 93-108 www. elsevier. com/locate/j marsy s Importance of heterotrophic bacterial assimilation of ammonium and nitrate in the Barents Sea during summer A.E. Allen a’b, M.H. Howard-Jones b’c, M.G. Booth b, M.E. Frischerb, P.G. Verity b’*, D.A. Bronkd, M.P. Sandersond aInstitute o f Ecology, University o f Georgia, Athens, GA 30602, USA hSkidaway Institute o f Oceanography, 10 Ocean Science Circle, Savannah, G A 31411, USA cGeorgia Institute o f Technology, Atlanta, GA 30338, USA Virginia Institute o f Marine Sciences, Gloucester Point, VA 23062, USA Received 6 July 2001; accepted 15 February 2002 Abstract In a transect across the Barents Sea into the marginal ice zone (MIZ), five 24-h experimental stations were visited, and uptake rates of NH j and NO3 by bacteria were measured along with their contribution to total dissolved inorganic nitrogen (DIN) assimilation. The percent bacterial DIN uptake of total DIN uptake increased substantially from 10% in open Atlantic waters to 40% in the MIZ. The percentage of DIN that accounted for total bacterial nitrogen production also increased from south to north across the transect. On average, at each of the five 24-h stations, bacteria accounted for 16-40% of the total NO3 uptake and 12-40% of the total N H | uptake. As a function of depth, bacteria accounted for 17%, 23%, and 26% of the total NHj assimilation and 17%, 37%, and 36% of the total NO7 assimilation at 5, 30, and 80 m, respectively. Bacteria accounted for a higher percentage of total NO3 uptake compared to total NHj uptake in 12 out of 15 samples. Bacterial productivity explains a substantial amount of the variability associated with bacterial DIN uptake, but the relationship between bacterial production and bacterial DIN uptake is best explained when the data from the open Atlantic water stations are grouped separately from the MIZ stations. The percentage of DIN that accounts for bacterial N production is approximately four-fold higher in 24 h MIZ stations compared with open Atlantic stations. This suggests that bacteria play a larger role in3 NO utilization, particularly in the MIZ, than previously hypothesized and that bacterial uptake of7 NOshould not be ignored in estimates of new production. Understanding processes that affect autotrophic based new production, such as heterotrophic bacterial utilization of NO3 , in polar oceans is of particular significance because of the role these regions may play in sequestering C 02. © 2002 Elsevier Science B.V. All rights reserved. Keywords: Nitrogen cycle; Nitrate; Arctic; New production; Heterotrophic bacteria; Microbial loop; 15N 1. Introduction * Corresponding author. Tel, +1-912-598-2376; fax: +1-912- The P1'“" 31? role ° f heterotrophic bacteria is clas- 598-2310. sically considered to be the decomposition and min- E-mail address: [email protected] (RG. Verity). eralization of dissolved and particulate organic 0924-7963/02/$ - see front matter © 2002 Elsevier Science B.V. All rights reserved. PII: S0924-7963(02)00171-9 94 A.E. Allen et al. / Journal o f Marine Systems 38 (2002) 93-108 nitrogen (DON and PON) (Pomeroy, 1974). The role are required to produce large amounts of sinking of heterotrophic bacteria in the consumption of a particles (Kirchman, 2000). significant fraction of the total NO3 or NH4 flux in Understanding the variability and magnitude of marine environments is seldom considered in pelagic new production in the polar regions is of particular carbon and nitrogen cycling models (Fasham et al., interest because of the role these regions may play in 1990; Bissett et al., 1999; Haupt et al., 1999). sequestering CO2 (Sarmiento and Toggweiler, 1984; Several studies have documented high rates of Walsh, 1989; Erickson et al., 1990). Studies in the NO 3 utilization by bacteria (Parker et al., 1975; Northern Bering Sea, the Chukchi Sea, and the Parsons et al., 1980; Horrigan et al., 1988; Kirchman Barents Sea have measured some of the highest et al., 1991), but only a few have attempted to primary production rates in the world’s oceans (Sam- measure bacterial inorganic nitrogen utilization brotto et al., 1984; Olsson et al., 1999; Luchetta et al., directly by separating the bacterial size fraction after 2000). Although there is considerable disagreement incubation in the presence 15N tracers (Harrison and over the role of bacteria in these cold waters (Pomeroy Wood, 1988; Probyn, 1990; Kirchman, 1994; Kirch­ and Deibel, 1986; Thingstad and Martinussen, 1991), man and Wheeler, 1998). One such study in the Arctic bacterioplankton appear to be important con­ Barents Sea estimated that 53% and 48% of NHj sumers of dissolved organic matter (Cota et al., 1990; and NO3 , respectively, was attributable to organisms Rivkin et al., 1996; Steward et al., 1996), but their <0.8 pm (Kristiansen et al., 1994). A recent review of contribution to total DIN utilization remains unclear. marine studies that have measured NH4 and NO3 Kirchman et al. (1989) found that about 50% of uptake by heterotrophic bacteria reports that bacteria heterotrophic bacteria from subarctic waters will pass account for 42% and 16% of NH4 and NO3 uptake, through GF/F filters (nominal pore size 0.7 pm). The respectively (Kirchman, 2000). purpose of this study was to more accurately estimate Significant heterotrophic bacterial utilization of bacterial and eukaryotic uptake by using0 . 8 and0 . 2 dissolved inorganic nitrogen (DIN) would have pro­ pm silver membrane filters (see Materials and meth­ found effects on the fluxes of N and C in the water ods section). The rate and amount of DIN utilized by column (Kirchman et al., 1992; Kirchman, 1994). In bacterioplankton was determined along a transect that particular, NO 3 uptake by heterotrophic bacteria is began in the Southern Barenst Sea, crossed the Polar important because of its potential impact on estimates Front, and ended in the marginal ice zone (MIZ) of new production and on the relationship between dominated by Arctic water. new production and carbon export out of the euphotic zone (Legendre and Grosselin, 1989; Kirchman, 2000). The magnitude of the vertical flux is thought 2. Materials and methods to be determined by new production, and biogenic matter vertical flux dynamics in the Barents Sea has Experiments were conducted during a cruise (ALV- been investigated previously (Wassmann et al., 1990, 3) aboard the R/V Jan Mayen in July 1999. Five 1993; Andreassen et al., 1996, 1999). stations (Fig. 1) were sampled over a 24 h period The traditional view of the marine nitrogen cycle along a transect beginning in 80% ice cover on July 1 holds that the downward flux of particulate nitrogen (78° 13.67' N, 34°23.02' E) and ending in the south­ would have to equal NO 3 uptake at steady state ern Barents Sea on July 9 (73°47.99' N, 31 °44.10' E). regardless of which group of microbes is using the The stations are referred to as Stns. I-V from south to NO 3 (Bronk et al., 1994; Kirchman, 2000). What is north. Water samples were collected using 10 L not appreciated or understood, however, is the extent Niskin bottles. to which bacteria might cause the system to deviate from steady state or to at least complicate this picture 2.1. Uptake o f inorganic nitrogen experimen ts by substantial utilization of NO3 in the euphotic zone. NO 3 uptake by bacteria could potentially uncouple At each station, 15N tracer techniques were used to new and export production by directing more carbon estimate uptake rates of NO 3 and NH4 into the >0.8 into the microbial loop where more trophic transfers and <0.8 pm size-fractions at 5 m, 30 m and 80 m. A.E. Allen et al. / Journal o f Marine Systems 38 (2002) 93-108 95 80°N 78°N 76°N 74°N 72DN 20°E 30°E 40°E 50°E Fig. 1. A map of the cmise track of the R/V Jan Mayen and locations of the five 24-h experimental stations (I-V) in July 1999. Nutrient concentrations from the literature were used Incubations were done in 1 liter polycarbonate to estimate 15N additions that would yield approx­ bottles in on-deck flow-through incubators under imately 10% enrichment over ambient levels. For simulated in situ light and temperature conditions. NO 3 and NH4 , the enrichments were 0.01, 0.1, and Whole water (unfractionated) and fractionated treat­ 0.6 pM and 0.01, 0.01, and 1 pM at 5, 30, and 80 m, ments for NO3 and NHj uptake experiments were respectively. For the most part, target enrichment prepared from samples collected at each depth. The levels were achieved to within 1.0 pM. At no time, fractionated treatment consisted of water that was however, did the 15N additions result in enrichments gently filtered (<5 in. Hg) through a 1.0-pm filter of over 10% of ambient NHj or NO3 concentra­ prior to incubation. Incubations lasted 3 h in order to tions. minimize the risk of substrate depletion. 96 A.E. Allen et al. / Journal o f Marine Systems 38 (2002) 93-108 The incubations were terminated by passing the production assuming 1.15 x IO17 cells mol~ 1, which whole-water samples through a 0 .8 -pm silver filter is the mean of all open oceanic studies (Ducklow and (Osmonics, Minnetonka, MN) to collect the 15N Carlson, 1992; Kirchman, 1992). Bacterial carbon labeled particulate nitrogen in the 0>.8 -pm size class. content for Barents Sea bacterioplankton was assumed The filtrate from these samples was collected and to be 15 fg C cell ~ 1 (Fagerbakke et al., 1996).
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