Bottom-up and top-down control of heterotrophic bacterioplankton growth in a phosphorus-depleted subtropical estuary, Florida Bay, USA

Williams, Clayton J.; Lavrentyev, Peter J.; Jochem, Frank J.

doi:10.3354/meps07697

Cited by 10 publications

(12 citation statements)

References 44 publications

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“…In such oligotrophic environments, LNA cells are therefore an important dynamic group, whose role in the microbial communities and in C cycling is far from negligible. This agrees with other studies showing that significant growth rates, sometimes equal to those of HNA cells, were also measured in LNA cells (Scharek and Latasa, 2007;Williams et al, 2008). LNA cells were found to be active members of the Hprok community, not only in terms of protein synthesis, but also in cell division, as shown in groups sorted following thymidine incorporation (Longnecker et al, 2006).…”

Section: Importance Of Lna Cells In the Leucine Incorporation Ratessupporting

confidence: 80%

Flow cytometric assessment of specific leucine incorporation in the open Mediterranean

et al. 2011

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Abstract. The surface of the Mediterranean Sea is a lowphosphate-low-chlorophyll marine area where marine heterotrophic prokaryotes significantly contribute to the biogeochemical cycles of all biogenic elements such as carbon, notably through the mineralization of dissolved organic compounds. Cell-specific leucine incorporation rates were determined in early summer in the open stratified Mediterranean Sea. The bulk leucine incorporation rate was on average 5 ± 4 pmol leu l −1 h −1 (n = 30). Cell-specific 3 Hleucine incorporation rates were assayed using flow cytometry coupled to cell sorting. Heterotrophic prokaryotes (Hprok) were divided into cytometric groups according to their side scatter and green fluorescence properties: high nucleic acid containing cells (HNA) with high scatter (HNAhs) and low scatter (HNA-ls) and low nucleic acid containing cells (LNA). Cell-specific leucine incorporation rates of these cytometric groups ranged from 2 to 54, 0.9 to 11, and 1 to 12 × 10 −21 mol cell −1 h −1 , respectively. LNA cells represented 45 to 63% of the Hprok abundance, and significantly contributed to the bulk leucine incorporation rates, from 12 to 43%. HNA/LNA ratios of cell-specific leucine incorporation were on average 2.0 ± 0.7 (n = 30). In surface layers (from 0 m down to the deep chlorophyll depth, DCM), cell-specific rates of HNA-hs were elevated (7 and 13 times greater than LNA and HNA-ls, respectively). Nevertheless, on average HNA-hs (26%) and LNA (27%) equally contributed to the bulk leucine incorporation in these layers. Prochlorococcus cells were easily sorted near the DCM and displayed cell-specific leucine incorporation rates ranging from 3 to 55 × 10 −21 mol leu cell −1 h −1 , i.e. as high asCorrespondence to: A. Talarmin (agathe.talarmin@univmed.fr) HNA-hs'. These sorted groups could therefore be defined as key-players in the process of leucine incorporation into proteins. The mixotrophic features of certain photosynthetic prokaryotes and the high contribution of LNA cells to leucine incorporation within the microbial communities of the Mediterranean could be reinforced.

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Section: Importance Of Lna Cells In the Leucine Incorporation Ratessupporting

confidence: 80%

Flow cytometric assessment of specific leucine incorporation in the open Mediterranean

et al. 2011

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“…6), as previously reported by Williams et al (2008). However, recent work indicates that gross growth rates of HNA cells are frequently 1 order of magnitude higher than those of LNA cells: differences of 3-to 5-fold higher values were reported in direct comparisons of HNA versus LNA bacteria ) and of phylo genetic groups ascribed to one or the other flow cytometric clusters (Teira et al 2009, Ferrera et al 2011.…”

Section: Lna and Hna Bacterial Apparent Net Growth Ratesmentioning

confidence: 73%

Dynamics of heterotrophic bacteria in temperate coastal waters: similar net growth but different controls in low and high nucleic acid cells

Huete‐Stauffer¹,

Morán

2012

Aquat. Microb. Ecol.

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) were similar for LNA and HNA cells, although related to different factors. LNA bacteria net growth rates were strongly positively correlated with temperature (r = 0.95, p < 0.01, n = 6) and negatively with chlorophyll a (r = −0.90, p = 0.01, n = 6), supporting the hypothesis that they are independent from phytoplankton, which was recently suggested for this and other coastal sites using different approaches. We also show an opposite relationship between cell size and apparent net growth rates of LNA and HNA bacteria, providing further evidence of fundamentally different ecological roles. KEY WORDS: Bacterioplankton · Nucleic acid content · Net growth rates · Coastal waters · Bay of Biscay Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 67: [211][212][213][214][215][216][217][218][219][220][221][222][223] 2012 the phylogenetic, physiological or ecological level of organization (e.g. Zubkov et al. 2001, Bouvier et al. 2007.Initially, HNA and LNA cells were grossly considered as the active and the inactive fractions, respectively, of the bacterial assemblage (Jellett et al. 1996, Lebaron et al. 2001. Indeed, HNA cells were usually much more correlated to bacterial production and bulk specific growth rates than LNA cells (Lebaron et al. 2001, Servais et al. 2003, whereas LNA bacteria were considered as dormant or dead cells , Vaqué et al. 2001, Lebaron et al. 2002. This initial picture is rapidly evolving, and LNA bacteria may present growth rates as high as the HNA subgroup (Zubkov et al. 2001, Longnecker et al. 2005, Nishimura et al. 2005 in environments such as the Mediterranean deep chlorophyll maximum (Scharek & Latasa 2007) or stratified waters of the Celtic Sea (Zubkov et al. 2001). LNA bacteria have been also predominantly associated with SAR11 and SAR86 clades, while Gammaproteobacteria and Bacteroidetes are usually only found as HNA cells (Mary et al. 2006, Teira et al. 2009, Schattenhofer et al. 2011, Vila-Costa et al. 2012, thus suggesting completely different phylogenetic compositions.Total abundance of heterotrophic bacteria is assumed to vary little across a wide range of aquatic environments (Ducklow 2000, Smith & del Giorgio 2003 from a few hundreds of thousands to a few million cells ml −1. Despite the constancy at ca. 10 6 cells ml −1 in surface seawater, natural bacterial communities show fluctuations in response to bottom-up (substrate availability) and top-down (grazing and viral pressure) control mechanisms as well as temperature (e.g. Pernthaler et al. 1996, Gasol & Duarte 2000, Pomeroy & Wiebe 2001, Morán et al. 2010. Recent work has shown that the dynamics of the HNA and LNA subgroups vary across environments and even shift seasonally within the same environment (Scha rek & Latasa 2007, Ortega-Retuerta et al. 2008, Morán et al. 2010. Controlled experiments have attempted to isolate bottom-up (Bouvy et al. 2004, Wetz & Wheeler 2004) from top-down controls (Iriarte et al. 2008, Longnecker et al. 2010. However, both types of processes inte...

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“…LNA cells were not correlated to changes in grazing rate in experimental or in situ samples (Vaqué et al 2001). However, LNA cells can be grazed at rates which are higher than or equal to (Jochem et al 2004, Scharek & Latasa 2007 as well as lower than (Williams et al 2008) the grazing rates for HNA cells. What causes the different response of protist grazers to LNA cells is not yet clear.…”

Section: Introductionmentioning

confidence: 92%

Effect of top-down control on cell-specific activity and diversity of active marine bacterioplankton

Longnecker

Wilson²,

Sherr³

et al. 2010

Aquat. Microb. Ecol.

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Mortality processes such as grazing and viral lysis can alter both phylogenetic diversity and cell-specific activity of bacterioplankton. We conducted experiments to examine the effect of reduction in grazer or viral abundance on metabolically active bacterioplankton at a eutrophic shelf station and an oligotrophic basin station. Leucine assimilation was used as a proxy to characterize metabolically active bacterial cells. The phylogenetic affiliation of marine bacterioplankton assimilating leucine was identified with fluorescence in situ hybridization and microautoradiography. Flow cytometric sorting of leucine-labeled cells quantified cell-specific activity of high nucleic acid (HNA) and low nucleic acid cells. The activity and diversity of the bacterial community at the oligotrophic station was more responsive to a reduction in mortality compared to the community at the eutrophic station. HNA cells at the oligotrophic station showed a 4-fold increase in cell-specific leucine incorporation when the abundance of flagellates was reduced and an 8-fold increase when the abundance of flagellates, viruses, and bacterial cells was reduced. The abundance of active Alphaproteobacteria increased at the oligotrophic station when either grazer or viral abundance was reduced. Activity responses were less striking at the eutrophic station, and the abundance of active Gammaproteobacteria showed a greater increase with reduced flagellates compared to the treatment with reduced flagellates, viruses, and bacterioplankton. Our results indicate both the presence and type of mortality process play a key role in structuring a bacterial community, and this effect varies in ecosystems of differing trophic state.KEY WORDS: Marine bacterioplankton · Top-down control · Leucine incorporation · Flow cytometry · Microautoradiography · Fluorescence in situ hybridization · Grazing · Viral lysis Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 58: [153][154][155][156][157][158][159][160][161][162][163][164][165] 2010 Protocols involving a combination of fluorescence in situ hybridization (FISH) with microautoradiography allow identification of metabolically active phylogenetic groups within marine bacterioplankton (e.g. Ouverney & Fuhrman 1999, Cottrell & Kirchman 2000. This approach has provided important insights into both spatial (Elifantz et al. 2007, Varela et al. 2008) and temporal (Alonso-Sáez & Gasol 2007) variability in the diversity of active bacterial cells. In previous work in the Oregon upwelling system, we found little spatial variability in the diversity of active cells (Longnecker et al. 2005), although the abundance of active cells increased with ecosystem trophic state (Longnecker et al. 2006a). These findings raised the question of the relative importance of top-down (mortality) versus bottom-up (substrate availability) processes in eutrophic compared to oligotrophic marine ecosystems.In addition to the qualitative information derived from FISH analysis, flow cyto...

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Bottom-up and top-down control of heterotrophic bacterioplankton growth in a phosphorus-depleted subtropical estuary, Florida Bay, USA

Cited by 10 publications

References 44 publications

Flow cytometric assessment of specific leucine incorporation in the open Mediterranean

Flow cytometric assessment of specific leucine incorporation in the open Mediterranean

Dynamics of heterotrophic bacteria in temperate coastal waters: similar net growth but different controls in low and high nucleic acid cells

Effect of top-down control on cell-specific activity and diversity of active marine bacterioplankton

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