Persistent El Niño driven shifts in marine cyanobacteria populations

Abstract

In the California Current Ecosystem, El Niño acts as a natural phenomenon that is partially representative of climate change impacts on marine bacteria at timescales relevant to microbial communities. Between 2014-2016, the North Pacific warm anomaly (a.k.a., the "blob") and an El Niño event resulted in prolonged ocean warming in the Southern California Bight (SCB). To determine whether this "marine heatwave" resulted in shifts in microbial populations, we sequenced the rpoC1 gene from the biogeochemically important picocyanobacteria Prochlorococcus and Synechococcus at 434 time points from 2009-2018 in the MICRO time series at Newport Beach, CA. Across the time series, we observed an increase in the abundance of Prochlorococcus relative to Synechococcus as well as elevated frequencies of ecotypes commonly associated with low-nutrient and high-temperature conditions. The relationships between environmental and ecotype trends appeared to operate on differing temporal scales. In contrast to ecotype trends, most microdiverse populations were static and possibly reflect local habitat conditions. The only exceptions were microdiversity from Prochlorococcous HLI and Synechococcus Clade II that shifted in response to the 2015 El Niño event. Overall, Prochlorococcus and Synechococcus populations did not return to their pre-heatwave composition by the end of this study. This research demonstrates that extended warming in the SCB can result in persistent changes in key microbial populations.

Fig 1. Seasonal and interannual changes in environmental conditions and ecotype frequencies.

(A) Temperature (°C), nitrate and phosphate concentrations (μM), and the log₁₀-transformed ratio of Prochlorococcus sequence counts relative to Synechococcus sequence counts in the MICRO time series. (B) Interpolated relative abundance of rpoC1 reads taxonomically assigned to the six most abundant Prochlorococcus (Pro.) and Synechococcus (Syn.) ecotypes. The sampling dates are marked along the top of the time series. (C) Linear model regression coefficients for environmental variables and relative ecotype abundance as a function month and year (see Methods). A trend of 0 is marked with horizontal dashed lines.

Fig 2. Pearson correlation coefficients (r) between relative abundance trends and environmental trends.

The significance of each correlation is marked as p-value: * < 0.05, ** < 0.01, *** <0.001. Bars without a mark had a non-significant correlation.

Fig 3. Microdiversity clusters within the most abundant Prochlorococcus and Synechococcus ecotypes were temporally and statistically stable.

Dendrograms represent the average-linkage hierarchical clustering of single nucleotide polymorphisms (SNP) differences between a rpoC1 reference sequence and the majority consensus sequence at each sampling time point. Each row of the dendrogram represents the consensus rpoC1 sequence at a time point, where only SNPs (in comparison to the reference sequence) are depicted. Only time points where the ecotype was present are shown. The reference rpoC1 sequence is depicted at the top of each dendrogram. Reference genomes used to compare rpoC1 sequences included: HLI–MIT9515; LLI–NATL2A; HLII–MIT9301; Clade I–WH8016; Clade IV–CC9902; and, Clade II–CC9605. Within-cluster sum of squares was used to determine the optimum number of SNP-based clusters (i.e., haplotypes). Cluster labels (red) indicate bootstrapped Jaccard similarity values for the most stable clusters (values < 0.5 are unstable, 0.6–0.75 weak stability, 0.75–0.85 stable, and > 0.85 highly stable). Stable clusters are alternately shaded in grey for emphasis.

Fig 4. Prochlorococcus HLI haplotypes (Pro.HLI.1 and Pro.HLI.2) and Synechococcus II haplotypes (Syn.II.1 and Syn.II.2) showed significant shifts in composition across the time series.

(A) Interpolated relative abundance of the haplotypes. Samples with less than 10 reads were removed from the analysis. (B) Linear regression coefficients for monthly and yearly trends in the Pro.HLI.2 and Syn.II.2 haplotypes. (C) Pearson’s correlation coefficients (ρ) comparing haplotype to environmental monthly and yearly trends. The significance of each correlation is marked as p-value: * < 0.05. Bars without a mark had a non-significant correlation.

Fig 5. Comparison of Prochlorococcus HLII and Synechococcus Clade II rpoC1 highly conserved SNPs detected at the Newport MICRO times series and on Pacific Ocean cruise NH1418 (September-October 2014; 19.00°N, -158.00°W to -3.00°N, -149.67°W; 5m depth).

Newport and NH1418 samples largely clustered separately but had some overlap in SNPs. Samples with less than 10 sequences were removed from the analysis. Clade labels (red) indicate bootstrapped Jaccard similarity values for the most stable clusters with more than two samples (values < 0.5 are unstable, 0.6–0.75 weak stability, 0.75–0.85 stable, and > 0.85 highly stable).

Fig 6. Conceptual diagram of picocyanobacterial community shifts at the MICRO time series from 2009–2018.

Synechococcus cells are outlined in purple and Prochlorococcus cells are outlined in green. Blue cell shading indicates cold temperature-adapted ecotypes and yellow cell shading indicates warm temperature-adapted ecotypes. The blue line indicates the nitrate trend (N) and the red line indicates the temperature trend (T).