Eco-evolutionary significance of domesticated retroelements in microbial genomes

Paul, Blair G.; Eren, A. Murat

doi:10.1186/s13100-022-00262-6

Cited by 10 publications

(10 citation statements)

References 76 publications

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“…Table 9; fastANI groupings) , suggesting that some consistent phage particles were present across the transect. As past research shows that high phage relatedness selects for CRISPR-Cas systems (60, 81, 82), these data suggest that the T. thiebautii CRISPR-Cas system is defending against a relatively conserved phage group.…”

Section: Resultsmentioning

confidence: 55%

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Importance of Mobile Genetic Element Immunity in Numerically AbundantTrichodesmiumClades

Webb

Held

Zhao

et al. 2022

Preprint

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The colony-forming cyanobacteria Trichodesmium spp. are considered one of the most important nitrogen-fixing genera in the warm, low nutrient, open ocean. Despite this central biogeochemical role, many questions about their evolution, physiology, and trophic interactions remain unanswered. To address these questions, we describe the genetic potential of the genus via significantly improved genomic assemblies of strains Trichodesmium thiebautii H94, Trichodesmium erythraeum 2175, and 17 new Trichodesmium metagenome-assembled genomes (MAGs, >50% complete) from hand-picked, Trichodesmium colonies spanning the Atlantic Ocean. Phylogenomics identified ∼four N2 fixing clades of Trichodesmium across the transect, with T. thiebautii dominating the colony-specific reads. Pangenomic analyses showed that all T. thiebautii MAGs are enriched in defense mechanisms and encode a vertically inherited Type III-B Clustered Regularly Interspaced Short Palindromic Repeats and associated protein-based immunity system (CRISPR-Cas hereafter). Surprisingly, this CRISPR-Cas system was absent in all T. erythraeum genomes and MAGs, vertically inherited by T. thiebautii, and correlated with increased signatures of horizontal gene transfer. Multiple lines of evidence indicate that the CRISPR-Cas system is functional in situ: 1. Trichodesmium CRISPR spacer sequences with 100% identical hits to field-assembled, putative phage genome fragments were identified, 2. High Trichodesmium spacer sequence variability indicating rapid adaptation, and 3. metaproteomic and transcriptomic expression analyses detecting the CRISPR-Cas system components in Trichodesmium colonies from the Atlantic and Pacific Oceans. These data suggest that phage or mobile genetic element immunity in T. thiebautii could contribute to their success, gene diversity, and numerical dominance over T. erythraeum in the oceans, thus warranting further Trichodesmium virome investigations.Significance statementOur work identifies CRISPR-Cas immunity as a phylogenetically distinct, environmentally expressed factor in the speciation of closely related N2-fixing Trichodesmium clades. These findings suggest that differential phage predation and resistance could be a previously overlooked selective pressure in the genus, potentially leading to the current numerical dominance of T. thiebautii over T. erythraeum in the oceans. Furthermore, while the currently CO2-limited T. erythraeum is expected to be a ‘winner’ of anthropogenic climate change, their predicted higher phage sensitivity than T. thiebautii could challenge this outcome.

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Section: Resultsmentioning

confidence: 55%

“…As past research shows that high phage relatedness selects for CRISPR-Cas systems (60,81,82), these data suggest that the T. thiebautii CRISPR-Cas system is defending against a relatively conserved phage group.…”

Section: Trichodesmium Auxiliary Gene Content and Genomic Average Nuc...mentioning

confidence: 59%

Importance of Mobile Genetic Element Immunity in Numerically AbundantTrichodesmiumClades

Webb

Held

Zhao

et al. 2022

Preprint

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“…It is noteworthy that many of these putative phage genome fragments were detected multiple times from independently assembled TriCoLim stations (Supplementary Table 5; fastANI groupings), suggesting that some consistent phage particles were present across the transect. As past research shows that high phage relatedness selects for CRISPR-Cas systems [69,80,81], these data suggest that the T. thiebautii CRISPR-Cas system is defending against a relatively conserved phage group.…”

Section: One-quarter Of All Trichodesmium Mags Have Shared Gene Clustersmentioning

confidence: 59%

Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades

Webb

Held

Zhao

et al. 2023

ISME Communications

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The colony-forming cyanobacteria Trichodesmium spp. are considered one of the most important nitrogen-fixing genera in the warm, low nutrient ocean. Despite this central biogeochemical role, many questions about their evolution, physiology, and trophic interactions remain unanswered. To address these questions, we describe Trichodesmium pangenomic potential via significantly improved genomic assemblies from two isolates and 15 new >50% complete Trichodesmium metagenome-assembled genomes from hand-picked, Trichodesmium colonies spanning the Atlantic Ocean. Phylogenomics identified ~four N2 fixing clades of Trichodesmium across the transect, with T. thiebautii dominating the colony-specific reads. Pangenomic analyses showed that all T. thiebautii MAGs are enriched in COG defense mechanisms and encode a vertically inherited Type III-B Clustered Regularly Interspaced Short Palindromic Repeats and associated protein-based immunity system (CRISPR-Cas). Surprisingly, this CRISPR-Cas system was absent in all T. erythraeum genomes, vertically inherited by T. thiebautii, and correlated with increased signatures of horizontal gene transfer. Additionally, the system was expressed in metaproteomic and transcriptomic datasets and CRISPR spacer sequences with 100% identical hits to field-assembled, putative phage genome fragments were identified. While the currently CO2-limited T. erythraeum is expected to be a ‘winner’ of anthropogenic climate change, their genomic dearth of known phage resistance mechanisms, compared to T. thiebautii, could put this outcome in question. Thus, the clear demarcation of T. thiebautii maintaining CRISPR-Cas systems, while T. erythraeum does not, identifies Trichodesmium as an ecologically important CRISPR-Cas model system, and highlights the need for more research on phage-Trichodesmium interactions.

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“…However, long-read metagenomes of high sequencing depth across several sites in all three salt marshes would be needed to phase single nucleotide variants. Paul and Eren (67) recently used metagenomes to compare the variation in Trichodesmium erythraeum ’s DGR targets over a much larger spatial scale between the Pacific and Indian oceans. They showed the presence of distinct combinations of variants at these two locations, which is likely the result of differential selection.…”

Section: Discussionmentioning

confidence: 99%

“…Of note, our results showed some population heterogeneity in the disruption of DGR loci, demonstrating that they are under a balance between a relaxed selection allowing for the degradation of the system, and a selection for functional, diversifying systems. Regardless of the underlying mechanism, the spatial pattern of diversification highlights the importance of exploring DGR activity in various environmental or experimental conditions (20, 67).…”

Section: Discussionmentioning

confidence: 99%

Targeted hypermutation of putative antigen sensors in multicellular bacteria

Doré,

Eisenberg,

Junkins

et al. 2023

Preprint

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Diversity-generating retroelements (DGRs) are used by bacteria, archaea and viruses as a targeted mutagenesis tool. Through error-prone reverse transcription, DGRs introduce random mutations at specific genomic loci, enabling rapid evolution of these targeted genes. However, the function and benefits of DGR-diversified proteins in cellular hosts remains elusive. We find that 82% of DGRs from one of the major monophyletic lineages of DGR reverse transcriptases are encoded by multicellular bacteria, which often have two or more DGR loci in their genomes. Using the multicellular purple sulfur bacteriumThiohalocapsasp. PB-PSB1 as an example, we characterized nine distinct DGR loci that cumulatively lead to more than 10294possible different combinations of target polypeptides. With environmental metagenomes from individualThiohalocapsaaggregates, we show that most of PB-PSB1's DGR targets are diversified across its biogeographic range, with spatial heterogeneity in the diversity of each locus. In PSB1 and other members of this lineage of cellular DGRs, diversified target genes are associated with NACHT-domain anti-phage defenses and putative ternary conflict systems previously shown to be enriched in multicellular bacteria. We propose that these DGR-diversified target genes act as antigen sensors that confer a form of adaptive immunity to their multicellular consortia. These findings have implications for the emergence of multicellularity, as the NACHT-domain anti-phage systems and ternary systems share both domain homology and conceptual similarities with the innate immune and programmed cell death pathways of plants and metazoans.

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Eco-evolutionary significance of domesticated retroelements in microbial genomes

Cited by 10 publications

References 76 publications

Importance of Mobile Genetic Element Immunity in Numerically AbundantTrichodesmiumClades

Importance of Mobile Genetic Element Immunity in Numerically AbundantTrichodesmiumClades

Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades

Targeted hypermutation of putative antigen sensors in multicellular bacteria

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