Craig A. Carlson

Oceanic Bacterial Production

There has been an explosion of research on marine microbial foodweb processes in the past decade. Today it is widely accepted that about 50% of the primary production in marine and fresh water is processed by bacteria each day (Williams, 1981; Cole et al., 1988). This striking finding was stimulated, as others have noted, by the introduction of convenient methods for the estimation of microbial biomass and activities in natural waters. Hobbie et al. (1977) and Watson et al. (1977) demonstrated conclusively that bacterial populations in the sea were large. By 1980, in addition to the pioneering and prescient work by Sorokin (e.g., Sorokin, 1971, 1973), reports of bacterial production measurements had begun to emerge (Sieburth et al., 1977; Karl, 1979; Larsson and Hagstrom, 1979; Fuhrman and Azam, 1980). Brock (1971) and Sieburth (1977) wrote early reviews on the subject, and Pomeroy (1974) introduced the importance of marine microbial processes to a large audience. In this chapter we review recent research on bacterial production in the ocean. The emphasis is on the open sea, but we will also discuss other marine habitats, partly because there are still few comprehensive studies of oceanic bacterial production. There is an equally large and rapidly growing literature on bacterial production in fresh waters (Cole et al., 1988; Currie, 1990) which deserves a review of its own, as well as comparison with the marine findings (Hobbie, 1988). We will not review related work in sediments, nor for the most part, related work on bacteriovores.

Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry

The Bermuda Atlantic Time-series Study (BATS) commenced monthly sampling in October 1988 as part of the US Joint Global Ocean Flux Study (JGOFS) program. The goals of the US JGOFS time-series research are to better understand the basic processes that control ocean biogeochemistry on seasonal to decadal time-scales, determine the role of the oceans in the global carbon budget, and ultimately improve our ability to predict the effects of climate change on ecosystems. The BATS program samples the ocean on a biweekly to monthly basis, a strategy that resolves major seasonal patterns and interannual variability. The core cruises last 4-5 d during which hydrography, nutrients, particle flux, pigments and primary production, bacterioplankton abundance and production, and often complementary ancillary measurements are made. This overview focuses on patterns in ocean biology and biogeochemistry over a decade at the BATS site, concentrating on seasonal and interannual changes in community structure, and the physical forcing and other factors controlling the temporal dynamics. Significant seasonal and interannual variability in phytoplankton and bacterioplankton production, biomass, and community structure exists at BATS. No strong relationship exists between primary production and particle flux during the 10 yr record, with the relationship slightly improved by applying an artificial lag of 1 week between production and flux. The prokaryotic picoplankton regularly dominate the phytoplankton community; diatom blooms are rare but occur periodically in the BATS time series. The increase in Chi a concentrations during bloom periods is due to increases by most of the taxa present, rather than by any single group, and there is seasonal succession of phytoplankton. The bacterioplankton often dominate the living biomass, indicating the potential to consume large amounts of carbon and play a major ecological role within the microbial food web. Bacterial biomass, production, and specific growth rates are highest during summer. Size structure and composition of the plankton community may be an important factor controlling the quality of dissolved organic matter produced and could affect production of bacterioplankton biomass. Larger heterotrophic plankton play an integral role in the flux of material out of the euphotic zone at BATS. Protozoans are abundant and can constitute a sizable component of sinking flux. Zooplankton contribute significantly to flux via production of rapidly sinking fecal pellets, and vertically migrating zooplankton can actively transport a significant amount of dissolved organic and inorganic carbon and nitrogen to deep water. An important question that remains to be further addressed at BATS is how larger climatological events drive some of the interannual variability in the biogeochemistry

Zooplankton vertical migration and the active transport of dissolved organic and inorganic carbon in the Sargasso Sea

The least known component of the “biological pump” is the active transport of carbon and nutrients by diel vertical migration of zooplankton. We measured CO2 respiration and dissolved organic carbon (DOC) excretion by individual species of common vertically migrating zooplankton at the US JGOFS Bermuda Atlantic Time-series Study (BATS) station. The inclusion of DOC excretion in this study builds on published research on active transport by respiration of inorganic carbon and allows a direct assessment of the role of zooplankton in the production of dissolved organic matter used in midwater microbial processes. On average, excretion of DOC makes up 24% (range=5–42%) of the total C metabolized (excreted+respired) and could represent a significant augmentation to the vertical flux that has already been documented for respiratory CO2 flux by migrant zooplankton. Migratory fluxes were compared to other transport processes at BATS. Estimates of combined active transport of CO2 and DOC by migrators at BATS averaged 7.8% and reached 38.6% of mean sinking POC flux at 150 m, and reached 71.4% of mean sinking POC flux at 300 m. DOC export by migrator excretion averaged 1.9% and reached 13.3% of annual DOC export by physical mixing at this site. During most of the year when deep mixing does not occur, diel migration by zooplankton could provide a supply of DOC to the deeper layers that is available for use by the microbial community. A carbon budget comparing migrant zooplankton transport to the balance of fluxes in the 300–600 m depth strata at BATS shows on average that the total migrant flux supplies 37% of the organic carbon remineralized in this layer, and that migrant DOC flux is more than 3 times the DOC flux gradient by diapycnal mixing. New estimates of active transport of both organic and inorganic carbon by migrants may help resolve observed imbalances in the C budget at BATS, but the magnitude is highly dependent on the biomass of the migrating community.

Dissolved organic carbon in the upper ocean of the central equatorial Pacific Ocean, 1992: Daily and finescale vertical variations

Detailed depth profiles of dissolved organic carbon (DOC) were determined at the JGOFS Equatorial Pacific Time Series site at 0°, 140°W in March/April and October 1992. DOC concentrations in the top 200 m, determined with the high temperature combustion (HTC) method, showed no elevated values over previous wet chemical estimates and ranged from an average of 67 μM C in the surface waters to 46 μM C at 200 m. The average integrated DOC concentration over 200 m was 11.4 mol C m−2 in March/April and 11.0 mol C m−2 in October. Variability frequency (i.e. seasonal) was minimal despite large changes in many biogeochemical parameters. Vertical distribution of DOC was highly correlated with physical properties and remained relatively independent of biological properties. High frequency variability appeared to be governed by physical processes. DOC production and consumption in the equatorial Pacific were tightly coupled, resulting in little accumulation and export of labile DOC.

Analyses of dissolved organic carbon in seawater: the JGOFS EqPac methods comparison

Abstract Results of a dissolved organic carbon (DOC) methods comparison are presented here in which five high temperature combustion (HTC) instruments and a wet chemical oxidation (WCO) method were used on a series of oceanic samples. The samples were collected during US JGOFS Equatorial Pacific Ocean cruises (EqPac) and most of the authors were involved with DOC analyses for the EqPac Program. Samples were collected with a “clean” protocol and were immediately quick frozen in replicate sample bottles. They were distributed by the first author to the other authors for “blind” analyses later on land on the stored samples. Comparable results (±7.5%) were found by three HTC instruments and the WCO method. There were difficulties with the other two HTC methods for which explanations and improvements are offered. The single most critical element for comparable DOC values appears to be assessment and subtraction of the total instrument blank (or reagent and handling blank for WCO methods). A “zero” carbon (very low C) water sample assisted in having all analysts achieve a uniform assessment of individual instrument or methods blanks. “Conditioning” of the catalyst bed in the combustion tube is critical to achieve consistent low instrument blanks. Failure to thoroughly condition the catalyst bed may be a significant error that can give erroneously high DOC values for oceanic samples. Reference standards available to all analysts also allowed comparison of instrument and methods performance. Contamination problems were demonstrated and it was shown that careful preparation and handling can reduce the potential for errors from contaminated samples. Results indicate that Equatorial Pacific oceanic DOC values in near surface waters are on the order of 60–70 μM C and deep water values on the order of 35–40 μM C. Since the “zero” carbon water contained a small, but measurable, amount of DOC, the sample values reported here may be slightly low. Because the lowest instrument blanks were equivalent to about 10 μM C, it is suggested that even if there were no instrument blank at all and all this “blank” were in the “zero” carbon water, the oceanic sample concentrations could not be underestimated by more than 10 μM C.

Stocks and dynamics of bacterioplankton carbon during the spring bloom in the eastern North Atlantic Ocean

Abstract Bacterial biomass increased five-fold in the euphotic zone (from 450 to 2250 mgC m−2) in response to the spring phytoplankton bloom in the eastern North Atlantic Ocean (Lat. 47°N, Long. 20°W) in 1989. Bacterial biomass accounted for about 20–30% of the particulate organic carbon (POC) above 50 m and a somewhat larger fraction in the layer below. Bacterial production averaged about 30% of primary production and remained rather constant while the primary production varied from 600 to 1500 mgC m−2 day−1 in response to event-scale changes in irradiance. Thus bacterial production varied from 15 to 80% of the concurrent primary production, with peaks occurring on overcast days when photosynthesis was low. Bacterial production in both the euphotic zone and the layer immediately below appeared to respond to the meteorologically-driven variations in photosynthesis with a time lag of 3–4 days, consistent with estimates of turnover rates of 0.2 day−1. In the upper layer incorporation of dissolved free amino acids supported about 20% of the production. The bacterial carbon demand at peak production required subsidies of carbon from the bulk POC and/or DOC pools. In the lower layer, decomposition of the vertical flux of sinking POC may have supported about half the mean production. Our bacterial production estimates for the 50–150 m layer are consistent with vertical flux estimates from drifting sediment traps and support other observations in suggesting that very large amounts of primary production pass through the DOC pool on short time-scales. Our observations suggest a spring-time North Atlantic condition for the microbial foodweb in which bacterial biomass makes up a relatively small part of the plankton carbon stock, but cycles rapidly (0.1–0.3 day−1) and commands a large share of the carbon cycling in the upper ocean. Through extensive metabolism of DOC and sinking POC in the upper 200 m, the bacterioplankton act as a selective gate through which some fraction of the products of primary production are exported into the oceanic interior.

Distribution of CO2 species, estimates of net community production, and air-sea CO2 exchange in the Ross Sea polynya

Measurements of surface total carbon dioxide (TCO2), alkalinity, and calculated pCO2, along with water column nutrients and hydrography, were made on two cruises to the Ross Sea polynya (NBP 94-6, November-December 1994 and NBP 95-8, December 1995 to January 1996). The polynya experiences an intense phytoplankton bloom during a short period of open water conditions from mid-December to mid-February each year. Our biogeochemical observations were used to determine the temporal variability of CO2, fluxes of carbon within the ocean, and rates of air-sea exchange of CO2. Depletions of TCO2, pCO2, and nitrate+nitrite were considerable (?70–150 ?mol kg?1, 80–150 ?atm, and 10–20 ?mol kg?1, respectively) and associated primarily with biological uptake during Phaeocystis and diatom blooms. Alkalinity was a conservative tracer of salinity and nitrate+nitrite. Surface ?CO2 was undersaturated by ?50–150 ?atm, and air-sea gas exchange of CO2 during open water conditions was directed from atmosphere to ocean. Observed surface stoichiometric C:N ratios were 6.66: 1 and 6.77:1 for the 2 years, consistent with global “Redfield” ratios, while C:P and N:P ratios were variable (75–141:1, 12–18:1). Estimates of net community production (NCP) rates were made using in situ changes in TCO2 and nitrate+nitrite across repeated transects along 76°30?S. Mean NCP rates across the polynya ranged from 0.86 to 0.98 g C m?2 d?1. These values may be underestimated by 5–25% because of the contribution of atmospheric CO2 to the surface layer through gas exchange. Export of carbon from the surface to depth was at least 55–60% of NCP rates.

Glucose fluxes and concentrations of dissolved combined neutral sugars (polysaccharides) in the Ross Sea and Polar Front Zone, Antarctica

We hypothesized that dissolved carbohydrates would be large components of the labile dissolved organic carbon (DOC) pool and would support much bacterial growth in Antarctic waters, especially the Ross Sea, since previous work had observed extensive phytoplankton blooms with potentially high production rates of carbohydrates in Antarctic seas. These hypotheses were tested on cruises in the Ross Sea and Antarctic Polar Front Zone as part of the US JGOFS program. Concentrations and fluxes of free glucose (the only free sugar detected) were very low, but dissolved polysaccharides appeared to be important components of the DOC pool. Concentrations of dissolved combined neutral sugars increased >3-fold during the phytoplankton bloom in the Ross Sea and were a large fraction (ca. 50%) of the semi-labile fraction of DOC. The relatively high concentrations of dissolved combined neutral sugars, which are thought to be quite labile, appear to explain why DOC accumulated during the phytoplankton bloom was degraded so quickly once the bloom ended. Some of the polysaccharides appeared to be more refractory, however, since dissolved combined neutral sugars were observed in deep waters (>550 m) and in early spring (October) in the Ross Sea, apparently having survived degradation for >8 months. The molecular composition of these refractory polysaccharides differed from that of polysaccharides sampled during the phytoplankton bloom. Fluxes of DOC were low in the Ross Sea compared to standing stocks and fluxes of particulate material,

The seasonal development of the bacterioplankton bloom in the Ross Sea, Antarctica, 1994-1997

We report on investigations of bacterioplankton growth dynamics and carbon utilization in the full water column of the Ross Sea, Antarctica carried out on six cruises in 1994–1997, using epifluorescence microscopy, thymidine and leucine incorporation to estimate bacterial abundance and production, respectively. The Ross Sea experienced a bacterial bloom with an amplitude equaling similar blooms observed in the North Atlantic and North Pacific, reaching 3 � 10 9 cells l � 1 or 35 mmol C m � 2 in late January. Increases in bacterial biomass were driven both by increases in abundance and in cell volume. Cell volumes ranged from 0.03mm 3 cell � 1 in early spring to over 0.15mm 3 cell � 1 in midsummer. Larger cells were associated with faster division rates. Bacterial growth rates ranged 0.02–0.3 divisions d � 1 , equal to rates at lower latitudes. Bacterial biomass accumulated steadily in the upper water column at a net rate of 0.03 d � 1 . While there is clear evidence of a bacterial bloom in the Ross Sea, equal to bacterioplankton blooms observed in other oceanic systems, the magnitude of bacterial response relative to the phytoplankton bloom was modest. For example, euphotic zone bacterial production (BP) rates were equivalent to 1–10% of particulate primary production (PP) except in April 1997 when PP was very low and BP : PP was sometimes >1. BP integrated over the upper 300 m was a more substantial fraction of the overlying PP than BP in the euphotic zone alone, with bacterial carbon demand in the upper 300 m about 30% of the seasonal PP. There was significant seasonal variation of bacterial biomass below the euphotic zone, indicating dynamic bacterial growth in the lower layer, and a supply of labile organic matter for bacteria. Bacterial metabolism is apparently limited by DOC flux in the upper layer. There is little evidence of temperature limitation, independent of substrate concentration. The relatively small diagenesis of phytoplankton biomass in the

CARBON PARTITIONING WITHIN PHAEOCYSTIS ANTARCTICA (PRYMNESIOPHYCEAE) COLONIES IN THE ROSS SEA, ANTARCTICA

The haptophyte Phaeocystis antarctica Karsten is a dominant species within the seasonal bloom in the Ross Sea. One of the unique characteristics of this form is that carbon is partitioned between the cells and the colonial matrix, a relationship that is poorly documented for this region. We combined particulate organic carbon measurements and microscopic analysis of P. antarctica‐dominated samples to assess the contribution of single cells, colony‐associated cells, and mucilage to the carbon concentrations of waters with P. antarctica. Two cruises to the Ross Sea were completed, one in austral spring 1994 and one in summer 1995–1996. In 1994 the bloom was dominated by colonial P. antarctica that contributed up to 96% of the total autotrophic carbon, whereas in 1995–1996 a mixture of P. antarctica and diatoms occurred. P. antarctica colony volume (V ) was related to colonial cell number (NC) by the relationship V = 417 ×NC1.67. Total colony carbon (CCOL) was calculated as the sum of cell carbon (CCC) and mucus‐related carbon (CM). We found the contribution of mucus carbon to be 213 ng C mm−3 of colony volume. For P. antarctica‐dominated assemblages sampled at the peak of the bloom, CM represented a minor fraction (14 ± 4%) of colony carbon, and during early summer conditions CM was at most 33% of CCOL. This organism plays a cardinal role in the carbon cycle of many regions. These results constrain the partitioning of carbon between cellular material and the colony matrix, information that is necessary to accurately describe the biogeochemical cycles influenced by this species.