Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades

Abstract

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.

Spatial and Temporal Resolution of Cyanobacterial Bloom Chemistry Reveals an Open-OceanTrichodesmium thiebautiias a Talented Producer of Specialized Metabolites

“…The HMG-CoA synthase was also identified in MAGs Bin1_Station19 and Bin1_Station18, which phylogenomics analysis supported as T. thiebautii. [43] Investigations of the assemblies of T. erythraeum IMS101 and the MAG assemblies from the field samples did not show these partial clusters described above but a different PKS-NRPS gene cluster was identified in T. erythraeum IMS101 and several of the field samples (Bin3_Station18_1, T. erythraeum; Bin4_Station16, T. erythraeum; Bin5_Station11, T.…”

“…). [43] Until there is an unequivocal biosynthetic identification of complete gene clusters in the T. thiebautii genomes, and the lack of these clusters in strains of T. erythraeum, no definitive answer can be given on species chemotaxonomy and metabologenomics. There is also previously published evidence that indicates environment populations are comprised of mixed species.…”

“…Examining collections from the GoM collected aboard NOAA's R/V Oregon II in 2021 (revisiting stations from 2019) and samples from the TriCoLim expedition, [43] we continued to identify the presence of metabolites from our 2014 library by matching MS/MS fragmentation patterns. The GoM samples showed the presence of certain trichophycins, smenamides, and other molecules (Table S3).…”

“…Genomic analysis of T. thiebautii H94, T. erythraeum IMS101, and field metagenomes. We examined several genome and metagenome assembled genomes (MAGs) that were publicly available, [43] searching for genetic architecture consistent with the unique functional groups (chlorovinylidene group and terminal vinyl chloride) present in T. thiebautii metabolites (although these functional groups were not in 1). We also examined genomes and MAGs from T. thiebautii and T. erythraeum for putative full biosynthetic gene clusters (BGCs) that might include 1.…”

“…We also examined genomes and MAGs from T. thiebautii and T. erythraeum for putative full biosynthetic gene clusters (BGCs) that might include 1. Specifically, this included the genomes of T. thiebautii H94, T. erythraeum IMS101, and the metagenome assemblies obtained from samples collected during the R/V Atlantis TriCoLim cruise, [43] having some colocation with the archived samples from the cruise that we analyzed chemically during this work. Analysis of PKS clusters present in the T. thiebautii H94 genome using the antiSMASH platform [44] and the known cluster BLAST function identified a module in the T. thiebautii H94 genome which showed similarity to modules in the curacin A pathway.…”