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1. Dual thermal ecotypes coexist within a nearly genetically identical population of the unicellular marine cyanobacterium Synechococcus

   https://doi.org/10.1073/pnas.2315701120  

   Kling, Joshua D. ; Lee, Michael D. ; Walworth, Nathan G. ; Webb, Eric A. ; Coelho, Jordan T. ; Wilburn, Paul ; Anderson, Stephanie I. ; Zhou, Qianqian ; Wang, Chunguang ; Phan, Megan D. ; et al ( November 2023 , Proceedings of the National Academy of Sciences)

   The extent and ecological significance of intraspecific functional 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 picocyanobacteriumSynechococcusisolated from a Narragansett Bay (RI) phytoplankton community thermal selection experiment. Thermal performance curves revealed selection at cool and warm temperatures had subdivided the initial population into thermotypes with pronounced differences in maximum growth temperatures. Curiously, the genomes of all 11 isolates were almost identical (average nucleotide identities of >99.99%, with >99% of the genome aligning) and no differences in gene content or single nucleotide variants were associated with either cool or warm temperature phenotypes. Despite a very high level of genomic similarity, sequenced epigenomes for two strains showed differences in methylation on genes associated with photosynthesis. These corresponded to measured differences in photophysiology, suggesting a potential pathway for future mechanistic research into thermal microdiversity. Our study demonstrates that present-day marine microbial populations can harbor cryptic but environmentally relevant thermotypes which may increase their resilience to future rising temperatures.

    

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2. MetaPop: a pipeline for macro- and microdiversity analyses and visualization of microbial and viral metagenome-derived populations

   https://doi.org/10.1186/s40168-022-01231-0  

   Gregory, Ann C. ; Gerhardt, Kenji ; Zhong, Zhi-Ping ; Bolduc, Benjamin ; Temperton, Ben ; Konstantinidis, Konstantinos T. ; Sullivan, Matthew B. ( December 2022 , Microbiome)

   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 autistic 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. 

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3. Seasonal environmental variability drives microdiversity within a coastal Synechococcus population

   https://doi.org/10.1111/1462-2920.15666  

   Hunter‐Cevera, Kristen R. ; Hamilton, Bryan R. ; Neubert, Michael G. ; Sosik, Heidi M. ( July 2021 , Environmental Microbiology)

   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.

    

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4. Parallel phylogeography of Prochlorococcus and Synechococcus

   https://doi.org/10.1038/s41396-018-0287-6  

   Kent, Alyssa G. ; Baer, Steven E. ; Mouginot, Céline ; Huang, Jeremy S. ; Larkin, Alyse A. ; Lomas, Michael W. ; Martiny, Adam C. ( October 2018 , The ISME Journal)

   The globally abundant marine Cyanobacteria Prochlorococcus and Synechococcus share many physiological traits but presumably have different evolutionary histories and associated phylogeography. In Prochlorococcus, there is a clear phylogenetic hierarchy of ecotypes, whereas multiple Synechococcus clades have overlapping physiologies and environmental distributions. However, microbial traits are associated with different phylogenetic depths. Using this principle, we reclassified diversity at different phylogenetic levels and compared the phylogeography. We sequenced the genetic diversity of Prochlorococcus and Synechococcus from 339 samples across the tropical Pacific Ocean and North Atlantic Ocean using a highly variable phylogenetic marker gene (rpoC1). We observed clear parallel niche distributions of ecotypes leading to high Pianka’s Index values driven by distinct shifts at two transition points. The first transition point at 6°N distinguished ecotypes adapted to warm waters but separated by macronutrient content. At 39°N, ecotypes adapted to warm, low macronutrient vs. colder, high macronutrient waters shifted. Finally, we detected parallel vertical and regional single-nucleotide polymorphism microdiversity within clades from both Prochlorococcus and Synechococcus, suggesting uniquely adapted populations at very specific depths, as well as between the Atlantic and Pacific Oceans. Overall, this study demonstrates that Prochlorococcus and Synechococcus have shared phylogenetic organization of traits and associated phylogeography.

    

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5. inStrain profiles population microdiversity from metagenomic data and sensitively detects shared microbial strains

   https://doi.org/10.1038/s41587-020-00797-0  

   Olm, Matthew R. ; Crits-Christoph, Alexander ; Bouma-Gregson, Keith ; Firek, Brian A. ; Morowitz, Michael J. ; Banfield, Jillian F. ( January 2021 , Nature Biotechnology)

   null (Ed.)

   Coexisting microbial cells of the same species often exhibit genetic variation that can affect phenotypes ranging from nutrient preference to pathogenicity. Here we present inStrain, a program that uses metagenomic paired reads to profile intra-population genetic diversity (microdiversity) across whole genomes and compares microbial populations in a microdiversity-aware man- ner, greatly increasing the accuracy of genomic comparisons when benchmarked against existing methods. We use inStrain to profile >1,000 fecal metagenomes from newborn premature infants and find that siblings share significantly more strains than unrelated infants, although identical twins share no more strains than fraternal siblings. Infants born by cesarean section har- bor Klebsiella with significantly higher nucleotide diversity than infants delivered vaginally, potentially reflecting acquisition from hospital rather than maternal microbiomes. Genomic loci that show diversity in individual infants include variants found between other infants, possibly reflecting inoculation from diverse hospital-associated sources. inStrain can be applied to any metagenomic dataset for microdiversity analysis and rigorous strain comparison. 

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