Diel partitioning in microbial phosphorus acquisition in the Sargasso Sea

Abstract

The daily cycle of photosynthetic primary production at the base of marine food webs is often limited by the availability of scarce nutrients. Microbial competition for these scarce resources can be alleviated insofar as the intensity of nutrient uptake and assimilation activities are distributed heterogeneously across organisms over periodic input cycles. Recent analysis of community transcriptional dynamics in the nitrogen-limited subtropical North Pacific gyre revealed evidence of temporal partitioning of nitrogen uptake and assimilation between eukaryotic phytoplankton, cyanobacteria, and heterotrophic bacteria over day-night cycles. Here, we present results from a Lagrangian metatranscriptomic time series survey in the Sargasso Sea and demonstrate temporally partitioned phosphorus uptake in this phosphorus-limited environment. In the Sargasso, heterotrophic bacteria, eukaryotic phytoplankton, and cyanobacteria express genes for phosphorus assimilation during the morning, day, and dusk, respectively. These results support the generality of temporal niche partitioning as an emergent mechanism that can structure uptake of limiting nutrients and facilitate coexistence of diverse microbes in open ocean ecosystems.

Keywords: biological oceanography; community ecology; microbial ecology.

Fig. 1.

Analysis of community-level diel gene expression. (A) Lagrangian cruise track with BATS station annotated in red and sampling locations annotated in black. Initial and final samples are labeled with local date and time. (B) Example gene transcript abundance time series for diel genes annotated as ABC-type transporters. Individual black lines represent the transcript abundance of one gene, the blue line represents a generalized additive model smoothing among all genes. Panels indicate the classification of genes by peak time as determined by the peak time analysis described in Methods. Shaded vertical bars indicate hours after sunset and before sunrise (18:00 to 06:00 local time).

Fig. 2.

Mean pairwise differences in peak timing for genes with diel expression across at least four distinct taxa. The X-axis indicates the number of cyanobacterial genera/heterotrophic bacterial orders/eukaryotic phyla with diel expression of a particular KEGG Orthologue as indicated by the periodicity analysis described in Methods. The Y-axis indicated the average difference in hours of the peak time of expression for each pair of orthologues (0 means all taxa have peak expression at the same time of day). Key genes in nitrogen assimilation and phosphorus assimilation are indicated. Orange point color indicates a gene with significantly (FDR = 10%) synchronized transcription. Synchronization was determined using a Monte Carlo–based simulation of the distribution of peak times observed in the full dataset, more details in Methods and detailed description of statistical framework in ref. (also see Dataset S4). Green points indicate a gene without synchronized transcription, labeled “asynchronous.”.

Fig. 3.

Temporal dynamics of phosphorus acquisition gene transcription. Each line plot shows the gene transcript abundance time series (z-score normalized by transcript and taxon) of a specific phosphorus-uptake related gene for a specific eukaryotic phylum or bacterial order (or cyanobacterial genus) identified as diel by the analysis described in Methods and available as Dataset S2. Information about detected but nondiel phosphorus uptake genes and diel analysis P-values are available in Dataset S5. Line color indicates the taxon expressing the transcript. Panels are divided horizontally by time of peak expression as calculated in methods, with 08:00 representing 8am local time, 12:00 noon local time, and so on. Shaded bars indicate hours between sunset and sunrise (18:00 to 06:00 local). Dashed lines are added to correspond to the peak time of genes in each panel. Panels are divided vertically by the species the gene is involved in transporting. The phosphate uptake category includes phosphate transporter subunits pstABC, pstS (KEGG K02036, K02037, K02038, K02040). The phosphonate uptake category includes the phosphonate transporter subunits phnCDE and putative phosphatase uptake subunits phnK, phnS (KEGG K02041, K02042, K02044, K05781, K11081)—pathway categorization for each gene and calculated peak time are presented in Dataset S3. Panels with no time series plotted indicate that there were no diel phosphate or phosphonate transporters with the labeled peak timing identified in any taxon in the dataset.