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Co-culture and biogeography of Prochlorococcus and SAR11 - PubMed

Co-culture and biogeography of Prochlorococcus and SAR11

Jamie W Becker et al. ISME J. 2019 Jun.

Abstract

Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15-70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11's central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 - highlighting the biogeochemical potential of these two groups.

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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1

Genome equivalents of Prochlorococcus and SAR11 relative to total identifiable bacteria and archaea in the surface ocean. (Upper) Locations of GEOTRACES, HOT and BATS Time-series, and Tara Oceans metagenome samples used for the analysis. (Lower) Vertical axes represent the abundance of Prochlorococcus (green) and SAR11 (red) genome equivalents relative to all other identifiable bacteria and archaea (gray) throughout the upper 50 m of the global ocean. GEOTRACES horizontal axes depict the distance along each transect, while the Tara Oceans horizontal axis displays evenly spaced samples organized by latitude (N to S) within each oceanic region. Forty degrees N/S are marked on the GA02 panel

Fig. 2
Fig. 2

Seasonality of Prochlorococcus (green) and SAR11 (red) estimated genome equivalents in metagenomes sampled from two ocean time series sites - the Bermuda Atlantic Time-series (BATS) and Hawaii Ocean Time-series (HOT). Vertical axes represent the abundance of each group (genome equivalents) relative to total identifiable bacteria and archaea genome equivalents, while horizontal axes represent time (month/year). Data are faceted by time series (horizontal) and depth (vertical). Surface samples are from within the mixed layer (≤25 m), DCM corresponds to the depth of maximum chlorophyll a fluorescence, and the base of the euphotic zone is defined by the depth at which ca. 1% of surface photosynthetically active radiation remains (see [33] for details). Solid lines represent a local weighted regression analysis (LOESS) smooth function for each taxonomic group at each depth. Anomalously low abundances of Prochlorococcus are sporadically observed in surface waters at the HOT study site

Fig. 3
Fig. 3

Cell abundance as a function of time in log-phase, semi-continuous batch co-cultures of SAR11 (Pelagibacterales sp. HTCC7211) (black lines) and Prochlorococcus strain MED4 (a; gray line) and MIT9313 (b; gray line) in ProMS medium. Dilution frequency and volume were dictated by Prochlorococcus cell density (see text)

Fig. 4
Fig. 4

Growth of Prochlorococcus strains MED4 a, MIT9312 b, MIT0801 c and MIT9313 (d; solid gray lines in a-d reproduced from Fig. S5) and SAR11 (Pelagibacterales sp. HTCC7211) (black lines) in co-culture compared to the growth of SAR11 monocultures (dashed gray lines). Growth curves for Prochlorococcus monocultures are presented in Fig. S5. Shaded regions denote the interval when Prochlorococcus are in stationary phase. SAR11 cells were undetectable in co-culture with Prochlorococcus after day 12–15 (dashed black arrows). Circles represent the mean (±s.d.) of biological triplicates. Error bars are smaller than the size of the symbols where not visible. Dot plot e depicts percent increases in SAR11 growth rate due to the presence of each Prochlorococcus strain. The growth rate of SAR11 alone was 0.41 day−1

Fig. 5
Fig. 5

Growth of Prochlorococcus (solid gray lines, reproduced from Fig. S7) and copiotrophic bacteria (black lines) in co-culture compared to the growth of copiotrophic bacterial monocultures (dashed gray lines). Growth curves for Prochlorococcus monocultures are presented in Fig. S7. Shaded regions denote the interval when Prochlorococcus are in stationary phase. Thalassospira MIT1351 monocultures were indistinguishable from instrument noise after day 7, precluding reliable determination of cell concentrations. Circles represent the mean (±s.d.) of biological triplicates. Error bars are smaller than the size of the symbols where not visible

Fig. 6
Fig. 6

Growth of SAR11 (Pelagibacterales sp. HTCC7211) monocultures in the presence (black lines) and absence (dashed gray lines) of pyruvate a and glycine b compared to growth of SAR11 in co-culture with Prochlorococcus strains MED4 (green lines) and MIT9313 (red lines) in the absence of pyruvate a and glycine b. Panel c shows the growth of SAR11 monocultures in the presence of methionine (black line) or 3-dimethylsulfoniopropionate (DMSP; dashed gray line) compared to growth of SAR11 in co-culture with MIT9313 in the presence of methionine (red line) or DMSP (dashed violet line). Circles represent the mean (±s.d.) of biological triplicates. Error bars are smaller than the size of the symbols where not visible. Dot plots on the right depict the maximum cell densities obtained for each treatment. Dots are colored to match the corresponding lines in the adjacent growth curves

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