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

   https://doi.org/10.1101/2020.05.27.119842  

   Kling, J ; Lee, M ; Webb, E ; Coelho, J ; Wilburn, P ; Anderson, S ; Zhou, Q ; Wang, C ; Phan, M ; Feu, F ; et al ( September 2020 , bioRxiv)

   null (Ed.)

   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. 

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2. 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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3. 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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4. Transcriptomic signatures of temperature adaptation in the eastern oyster Crassostrea virginica

   https://doi.org/10.1111/jeb.13789  

   Johnson, Kevin M. ; Jones, Hollis R. ; Casas, Sandra M. ; La Peyre, Jerome F. ; Kelly, Morgan W. ( July 2021 , Journal of Evolutionary Biology)

   The large geographic distribution of the eastern oyster,Crassostrea virginica,makes it an ideal species to test how populations have adapted to latitudinal gradients in temperature. Despite inhabiting distinct thermal regimes, populations ofC. virginicanear the species’ southern and northern geographic range show no population differences in their physiological response to temperature. In this study, we used comparative transcriptomics to understand how oysters from either end of the species’ range maintain enantiostasis across three acclimation temperatures (10, 20, and 30°C). With this approach, we identified genes that were differentially expressed in response to temperature between individuals ofC. virginicacollected from New Brunswick, Canada and Louisiana, USA. We observed a core set of genes whose expression responded to temperature in both populations, but also an even larger set of genes with expression patterns that were unique to each population. Intriguingly, the genes with population‐specific responses to temperature had elevatedF_STand Ka/Ks ratios compared to the genome‐wide average. In contrast, genes showing only a response to temperature were found to only have elevatedF_STvalues suggesting that divergentF_STmay be due to selection on linked regulatory regions rather than positive selection on protein coding regions. Taken together, our results suggest that, despite coarse‐scale physiological similarities, natural selection has shaped divergent gene expression responses to temperature in geographically separated populations of this broadly eurythermal marine invertebrate.

    

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5. Whole genome resequencing identifies local adaptation associated with environmental variation for redband trout

   https://doi.org/10.1111/mec.16810  

   Andrews, Kimberly R. ; Seaborn, Travis ; Egan, Joshua P. ; Fagnan, Matthew W. ; New, Daniel D. ; Chen, Zhongqi ; Hohenlohe, Paul A. ; Waits, Lisette P. ; Caudill, Christopher C. ; Narum, Shawn R. ( December 2022 , Molecular Ecology)

   Aquatic ectotherms are predicted to harbour genomic signals of local adaptation resulting from selective pressures driven by the strong influence of climate conditions on body temperature. We investigated local adaptation in redband trout (Oncorhynchus mykiss gairdneri) using genome scans for 547 samples from 11 populations across a wide range of habitats and thermal gradients in the interior Columbia River. We estimated allele frequencies for millions of single nucleotide polymorphism loci (SNPs) across populations using low‐coverage whole genome resequencing, and used population structure outlier analyses to identify genomic regions under divergent selection between populations. Twelve genomic regions showed signatures of local adaptation, including two regions associated with genes known to influence migration and developmental timing in salmonids (GREB1L,ROCK1,SIX6). Genotype–environment association analyses indicated that diurnal temperature variation was a strong driver of local adaptation, with signatures of selection driven primarily by divergence of two populations in the northern extreme of the subspecies range. We also found evidence for adaptive differences between high‐elevation desert vs. montane habitats at a smaller geographical scale. Finally, we estimated vulnerability of redband trout to future climate change using ecological niche modelling and genetic offset analyses under two climate change scenarios. These analyses predicted substantial habitat loss and strong genetic shifts necessary for adaptation to future habitats, with the greatest vulnerability predicted for high‐elevation desert populations. Our results provide new insight into the complexity of local adaptation in salmonids, and important predictions regarding future responses of redband trout to climate change.

    

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