SAR11 dominance among metabolically active low nucleic acid bacterioplankton in surface waters along an Atlantic meridional transect

Abstract

Low nucleic acid (LNA) bacterioplankton (sorted by flow cytometry) were characterised in surface water samples along a meridional transect from 48°N to 40°S across the Atlantic Ocean. The LNA bacterioplankton abundance and metabolic activity, assessed by their 35 S-methionine uptake rate, were similar along the transect, representing 36 ± 6 and 36 ± 11% of total bacterioplankton, respectively. Fluorescence in situ hybridisation analysis of the flow-sorted cells revealed that the LNA bacterioplankton population was dominated (59 ± 4%) by and contained virtually all the identifiable SAR11 clade cells throughout the Atlantic Ocean. Therefore, the present study provides ecological characterisation of this flow-sorted group and suggests both phylogenetic and functional constancy of the LNA bacterioplankton at the basin-scale. KEY WORDS: Flow cytometry sorting · Cell metabolic activity · SAR11 clade · CARD-FISH · Radioactive tracer labelling · Atlantic Ocean Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 45: [107][108][109][110][111][112][113] 2006 into the South Subtropical Frontal Zone (SSFZ, Belkin & Gordon 1996). As it was not possible to work on every sample collected along the transect, we selected representative samples for a basin-scale study. MATERIALS AND METHODSSampling area. The material was collected and measurements were made primarily on one Atlantic Meridional Transect (AMT) cruise on board the RRS 'James Clark Ross', cruise no. JR91, transect no. AMT-13, in September and October 2003 (Fig. 1). Up to 24 seawater samples were collected approximately every 12 h from a range of depths in the top 300 m using a rosette of 24 × 20 l Niskin bottles mounted on a conductivity-temperature-density (CTD) profiler. The Bpl cells were routinely fixed with 1% paraformaldehyde (PFA) final concentration.The abundance of Bpl was determined at every station , and for the present study 9 stations were chosen along the transect to represent the basin-scale range of surface waters (Fig. 1). The samples for the study of turnover rates of methionine (Met) by total bacterioplankton and by the LNA group sorted by flow cytometry were collected from depths of 3 to 7 m. Methionine uptake was chosen because of the high specific activity of the 35 S-methionine precursor and because previous studies have shown that microbial uptake of this amino acid are strongly correlated with the uptake of other amino acids such as leucine (Zubkov et al. 2004). The analyses also included the phylogenetic affiliation of the flow-sorted LNA cells using fluorescence in situ hybridisation (FISH). To test that the results obtained from the selected stations were representative of the Atlantic surface waters, an additional 15 stations ( Fig. 1) were included for comparison of the relative LNA abundance and Met uptake rates.Additional samples for phylogenetic analyses of bacterioplankton were collected from the Northern Atlantic at 5 stations on a later cruise on the RRS 'Discovery', cruise...

Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea

“…Abundance The high relative abundance of SAR11 cells we report for the BATS site is consistent with previous studies in the Sargasso Sea (Morris et al, 2002;Malmstrom et al, 2004), the eastern North Atlantic subtropical gyre (Mary et al, 2006) and the coastal oligotrophic Mediterranean Sea (Alonso-Saez et al, 2007). The ubiquity and numerical dominance of SAR11, supported by genomic and culture evidence revealing their metabolism Giovannoni et al, 2005a) and cell-specific radioactive substrate uptake experiments (Malmstrom et al, 2004;Mou et al, 2007) is compelling evidence that these cells play a major role in the oxidation of organic carbon in the oceans.…”

“…These organisms have the smallest genomes known for free-living heterotrophic cells, an apparent consequence of genome streamlining and reduction driven by the selection for efficient growth in oligotrophic ocean habitats (Giovannoni et al, 2005a). Mary et al (2006) found that SAR11 dominated the low nucleic acid fraction of bacterioplankton in the North Atlantic subtropical gyre, consistent with the prediction that small genomes are common to this clade.…”

Marine bacterial community structure resilience to changes in protist predation under phytoplankton bloom conditions

“…This progressive reduction in diversity could be related to the increase found in one Alphaproteobacteria family (i.e., the Rhodobacteraceae, increasing from 3% relative abundance at time 0 to 485% at day 8), at the expense of the Gammaproteobacteria, Cyanobacteria and SAR11 clade members. Several authors have found that SAR11 clade bacteria are large contributors to the LNA cells fraction in ocean environments (Fuchs et al, 2005;Longnecker et al, 2005;Mary et al, 2006;Vila-Costa et al, 2012). This is in agreement with the parallel reduction found in the number of LNA cells and in the relative abundance of SAR11 during the experiment.…”

Bias in assessments of marine microbial biodiversity in fosmid libraries as evaluated by pyrosequencing

“…However, no PCR cloning was used in this study, and the percentage hits to SAR11 from the sequencing of random fragments were similar to those enumerated using fluorescent in situ hybridization in surface water in other studies (Mary et al, 2006). It is clear that large fragment-length inserts of fosmid libraries confer a Figure 3 Fragment recruitment plots for key bacterioplankton species.…”

“…(Suzuki et al, 1997;Buchan et al, 2005). In contrast to an estimated 25% abundance of SAR11 in marine microbial communities from plasmid libraries (Giovannoni et al, 2005) and 12-37% abundance from direct counting of SAR11 using fluorescent in situ hybridization (Mary et al, 2006), Gilbert et al (2008) isolated only a single clone containing a 16S rRNA gene with homology to the SAR11 clade from a marine surface water fosmid library of 10 000 clones. It is interesting that this clone consisted largely of the 48-kb hypervariable region neighbouring the 16S rRNA gene, with a richer GC content than the GC-poor SAR11 core genome.…”