skip to main content

Title: Seasonal environmental variability drives microdiversity within a coastal Synechococcus population
Summary

Marine microbes often show a high degree of physiological or ecological diversity below the species level. This microdiversity raises questions about the processes that drive diversification and permit coexistence of diverse yet closely related marine microbes, especially given the theoretical efficiency of competitive exclusion. Here, we provide insight with an 8‐year time series of diversity withinSynechococcus, a widespread and important marine picophytoplankter. The population ofSynechococcuson the Northeast U.S. Shelf is comprised of six main types, each of which displays a distinct and consistent seasonal pattern. With compositional data analysis, we show that these patterns can be reproduced with a simple model that couples differential responses to temperature and light with the seasonal cycle of the physical environment. These observations support the hypothesis that temporal variability in environmental factors can maintain microdiversity in marine microbial populations. We also identify how seasonal diversity patterns directly determine overarchingSynechococcuspopulation abundance features.

Authors:
 ;  ;  ;  
Award ID(s):
1655686
Publication Date:
NSF-PAR ID:
10370491
Journal Name:
Environmental Microbiology
Volume:
23
Issue:
8
Page Range or eLocation-ID:
p. 4689-4705
ISSN:
1462-2912
Publisher:
Wiley-Blackwell
Sponsoring Org:
National Science Foundation
More Like this
  1. Summary

    TheSynechococcuscyanobacterial population at the Scripps Institution of Oceanography pier in La Jolla, CA, shows large increases in abundance, typically in the spring and summer followed, by rapid declines within weeks. Here we used amplicon sequencing of the ribosomal RNA internal transcribed spacer region to examine the microdiversity within this cyanobacterial genus during these blooms as well as further offshore in the Southern California coastal ecosystem (CCE). These analyses revealed numerousSynechococcusamplicon sequence variants (ASVs) and that clade and ASV composition can change over the course of blooms. We also found that a large bloom in August 2016 was highly anomalous both in its overallSynechococcusabundance and in terms of the presence of normally oligotrophicSynechococcusclade II. The dominant ASVs at the pier were found further offshore and in the California Current, but we did observe more oligotrophic ASVs and clades along with depth variation inSynechococcusdiversity. We also observed that the dominant sequence variant switched during the peak of multipleSynechococcusblooms, with this switch occurring in multiple clades, but we present initial evidence that this apparent ASV switch is a physiological response rather than a change in the dominant population.

  2. The extent and ecological significance of intraspecific diversity within marine microbial populations is still poorly understood, and it remains unclear if such strain-level microdiversity will affect fitness and persistence in a rapidly changing ocean environment. In this study, we cultured 11 sympatric strains of the ubiquitous marine picocyanobacterium Synechococcus isolated from a Narragansett Bay (Rhode Island, USA) phytoplankton community thermal selection experiment. Despite all 11 isolates being highly similar (with average nucleotide identities of >99.9%, with 98.6-100% of the genome aligning), thermal performance curves revealed selection at warm and cool temperatures had subdivided the initial population into thermotypes with pronounced differences in maximum growth temperatures. Within the fine-scale genetic diversity that did exist within this population, the two divergent thermal ecotypes differed at a locus containing genes for the phycobilisome antenna complex. Our study demonstrates that present-day marine microbial populations can contain microdiversity in the form of cryptic but environmentally-relevant thermotypes that may increase their resilience to future rising temperatures.
  3. Abstract

    Synechococcusis a widespread and important marine primary producer. Time series provide critical information for identifying and understanding the factors that determine abundance patterns. Here, we present the results of analysis of a 16‐yr hourly time series ofSynechococcusat the Martha's Vineyard Coastal Observatory, obtained with an automated, in situ flow cytometer. We focus on understanding seasonal abundance patterns by examining relationships between cell division rate, loss rate, cellular properties (e.g., cell volume, phycoerythrin fluorescence), and environmental variables (e.g., temperature, light). We find that the drivers of cell division vary with season; cells are temperature‐limited in winter and spring, but light‐limited in the fall. Losses to the population also vary with season. Our results lead to testable hypotheses aboutSynechococcusecophysiology and a working framework for understanding the seasonal controls ofSynechococcuscell abundance in a temperate coastal system.

  4. Abstract Background Microbes and their viruses are hidden engines driving Earth’s ecosystems from the oceans and soils to humans and bioreactors. Though gene marker approaches can now be complemented by genome-resolved studies of inter-(macrodiversity) and intra-(microdiversity) population variation, analytical tools to do so remain scattered or under-developed. Results Here, we introduce MetaPop, an open-source bioinformatic pipeline that provides a single interface to analyze and visualize microbial and viral community metagenomes at both the macro - and microdiversity levels. Macrodiversity estimates include population abundances and α- and β-diversity. Microdiversity calculations include identification of single nucleotide polymorphisms, novel codon-constrained linkage of SNPs, nucleotide diversity ( π and θ ), and selective pressures (pN/pS and Tajima’s D ) within and fixation indices ( F ST ) between populations. MetaPop will also identify genes with distinct codon usage. Following rigorous validation, we applied MetaPop to the gut viromes of autistic children that underwent fecal microbiota transfers and their neurotypical peers. The macrodiversity results confirmed our prior findings for viral populations (microbial shotgun metagenomes were not available) that diversity did not significantly differ between autistic and neurotypical children. However, by also quantifying microdiversity, MetaPop revealed lower average viral nucleotide diversity ( π ) in autisticmore »children. Analysis of the percentage of genomes detected under positive selection was also lower among autistic children, suggesting that higher viral π in neurotypical children may be beneficial because it allows populations to better “bet hedge” in changing environments. Further, comparisons of microdiversity pre- and post-FMT in autistic children revealed that the delivery FMT method (oral versus rectal) may influence viral activity and engraftment of microdiverse viral populations, with children who received their FMT rectally having higher microdiversity post-FMT. Overall, these results show that analyses at the macro level alone can miss important biological differences. Conclusions These findings suggest that standardized population and genetic variation analyses will be invaluable for maximizing biological inference, and MetaPop provides a convenient tool package to explore the dual impact of macro - and microdiversity across microbial communities.« less
  5. Abstract

    Hourly, year‐round flow cytometry has made it possible to relate seasonal environmental variability to the population dynamics of the smallest, most abundant phytoplankton on the Northeast US Shelf. To evaluate whether the insights from these data extend toSynechococcusfarther from shore, we analyze flow cytometry measurements made continuously from the underway systems on 21 cruises traveling between the Martha's Vineyard Coastal Observatory (MVCO) and the continental shelf break. We describe how seasonal patterns inSynechococcus, which have been documented in detail at MVCO, occur across the region with subtle variation. We find that the underlying relationship between temperature and division rate is consistent across the shelf and can explain much of the observed spatial variability in concentration. Connecting individual cell properties to annual and regional patterns in environmental conditions, these results demonstrate the value of autonomous monitoring and create an improved picture of picophytoplankton dynamics within an economically important ecosystem.