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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. 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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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. Target-enriched long-read sequencing (TELSeq) contextualizes antimicrobial resistance genes in metagenomes

   https://doi.org/10.1186/s40168-022-01368-y  

   Slizovskiy, Ilya B.; Oliva, Marco; Settle, Jonathen K.; Zyskina, Lidiya V.; Prosperi, Mattia; Boucher, Christina; Noyes, Noelle R. (December 2022, Microbiome)

   Abstract Background Metagenomic data can be used to profile high-importance genes within microbiomes. However, current metagenomic workflows produce data that suffer from low sensitivity and an inability to accurately reconstruct partial or full genomes, particularly those in low abundance. These limitations preclude colocalization analysis, i.e., characterizing the genomic context of genes and functions within a metagenomic sample. Genomic context is especially crucial for functions associated with horizontal gene transfer (HGT) via mobile genetic elements (MGEs), for example antimicrobial resistance (AMR). To overcome this current limitation of metagenomics, we present a method for comprehensive and accurate reconstruction of antimicrobial resistance genes (ARGs) and MGEs from metagenomic DNA, termed t arget- e nriched l ong-read seq uencing (TELSeq). Results Using technical replicates of diverse sample types, we compared TELSeq performance to that of non-enriched PacBio and short-read Illumina sequencing. TELSeq achieved much higher ARG recovery (>1,000-fold) and sensitivity than the other methods across diverse metagenomes, revealing an extensive resistome profile comprising many low-abundance ARGs, including some with public health importance. Using the long reads generated by TELSeq, we identified numerous MGEs and cargo genes flanking the low-abundance ARGs, indicating that these ARGs could be transferred across bacterial taxa via HGT. Conclusions TELSeq can provide a nuanced view of the genomic context of microbial resistomes and thus has wide-ranging applications in public, animal, and human health, as well as environmental surveillance and monitoring of AMR. Thus, this technique represents a fundamental advancement for microbiome research and application. 

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5. Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally occurring isolates of a model plant symbiont

   https://doi.org/10.1098/rspb.2022.0477  

   Batstone, Rebecca T.; Burghardt, Liana T.; Heath, Katy D. (July 2022, Proceedings of the Royal Society B: Biological Sciences)

   Given the need to predict the outcomes of (co)evolution in host-associated microbiomes, whether microbial and host fitnesses tend to trade-off, generating conflict, remains a pressing question. Examining the relationships between host and microbe fitness proxies at both the phenotypic and genomic levels can illuminate the mechanisms underlying interspecies cooperation and conflict. We examined naturally occurring genetic variation in 191 strains of the model microbial symbiont Sinorhizobium meliloti , paired with each of two host Medicago truncatula genotypes in single- or multi-strain experiments to determine how multiple proxies of microbial and host fitness were related to one another and test key predictions about mutualism evolution at the genomic scale, while also addressing the challenge of measuring microbial fitness. We found little evidence for interspecies fitness conflict; loci tended to have concordant effects on both microbe and host fitnesses, even in environments with multiple co-occurring strains. Our results emphasize the importance of quantifying microbial relative fitness for understanding microbiome evolution and thus harnessing microbiomes to improve host fitness. Additionally, we find that mutualistic coevolution between hosts and microbes acts to maintain, rather than erode, genetic diversity, potentially explaining why variation in mutualism traits persists in nature. 

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