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Summary Arbuscular mycorrhizal fungi (AMF) form beneficial associations with plants, and are thought to have been critical to the adaptation of the ancestor of terrestrial plants during the transition onto land. However, the ability of AMF to associate with aquatic plants is unclear. To address this, we used 65 publicly available genomes and transcriptomes (25 freshwater, 23 terrestrial and 17 marine plants) to interrogate the genomic potential to form AMF associations in aquatic plant lineages in the order Alismatales. We explored the presence or absence of homologs of 45 genes, with a a special focus on six critical genes including three that co-evolved with AMF associations (RAD1, STR1, STR2) and three necessary for intracellular symbiosis (SymRK, CCaMK/DMI3, CYCLOPS/IDP3). Our results indicate a pattern likely consistent with independent gene losses (or extreme divergence) of symbiosis genes across aquatic lineages suggesting a possible inability to form AMF associations. However, some of these conserved genes (i.e.,CCaMK/DMI3) are purported to function in other types of fungal symbioses, such as ectomycorrhizal symbiosis, and were observed here in a subset of aquatic lineages, including seagrasses. Overall, our findings highlight the complex evolutionary trajectories of symbiosis-related genes in aquatic plants, suggesting that while AMF associations may have been lost in certain lineages, others have genes that may allow them to form alternative fungal symbioses which may still play an underappreciated role in their ecology. 

Abstract Fungi play pivotal roles in terrestrial ecosystems as decomposers, pathogens, and endophytes, yet their significance in marine environments is often understudied. Seagrasses, as globally distributed marine flowering plants, have critical ecological functions, but knowledge about their associated fungal communities remains relatively limited. Previous amplicon surveys of the fungal community associated with the seagrass,Zostera marinahave revealed an abundance of potentially novel chytrids. In this study, we employed deep metagenomic sequencing to extract metagenome-assembled genomes (MAGs) from these chytrids and other microbial eukaryotes associated withZ. marinaleaves. Our efforts resulted in the recovery of five eukaryotic MAGs, including a single fungal MAG in the order Loubulomycetales (65% BUSCO completeness), three MAGs representing diatoms in the family Bacillariaceae (93%, 70% and 31% BUSCO completeness) and a single MAG representing a haptophyte algae in the genusPrymnesium(40% BUSCO completeness). Whole-genome phylogenomic assessment of these MAGs suggests they all largely represent under sequenced, and possibly novel eukaryotic lineages. Of particular interest, the chytrid MAG was placed within the order Lobulomycetales, consistent with the identity of the dominant chytrid from previousZ. marinaamplicon survey results. Annotation of this MAG yielded 5,650 gene models of which 77% shared homology to current databases. With-in these gene models, we predicted 121 carbohydrate-active enzymes and 393 secreted proteins (103 cytoplasmic effectors, 30 apoplastic effectors). Exploration of orthologs between the Lobulomycetales MAG and existing Chytridiomycota genomes have revealed a landscape of high-copy gene families related to host recognition and interaction. Further machine learning analyses based on carbohydrate-active enzyme composition predict that this MAG is a symbiont. Overall, these five eukaryotic MAGs represent substantial genomic novelty and valuable community resources, contributing to a deeper understanding of the roles of fungi and other microbial eukaryotes in the larger seagrass ecosystem. 

Abstract BackgroundSeagrasses are globally distributed marine flowering plants that play foundational roles in coastal environments as ecosystem engineers. While research efforts have explored various aspects of seagrass-associated microbial communities, including describing the diversity of bacteria, fungi and microbial eukaryotes, little is known about viral diversity in these communities. ResultsTo begin to address this, we leveraged metagenomic sequencing data to generate a catalog of bacterial metagenome-assembled genomes (MAGs) and phage genomes from the leaves of the seagrass,Zostera marina. We expanded the robustness of this viral catalog by incorporating publicly available metagenomic data from seagrass ecosystems. The final MAG set represents 85 high-quality draft and 62 medium-quality draft bacterial genomes. While the viral catalog represents 354 medium-quality, high-quality, and complete viral genomes. Predicted auxiliary metabolic genes in the final viral catalog had putative annotations largely related to carbon utilization, suggesting a possible role for phage in carbon cycling in seagrass ecosystems. ConclusionsThese genomic resources provide initial insight into bacterial-viral interactions in seagrass meadows and are a foundation on which to further explore these critical interkingdom interactions. These catalogs highlight a possible role for viruses in carbon cycling in seagrass beds which may have important implications for blue carbon management and climate change mitigation. 

Abstract Colletotrichumspp. have a complicated history of association with land plants. Perhaps most well-known as plant pathogens for the devastating effect they can have on agricultural crops, someColletotrichumspp. have been reported as beneficial plant endophytes. However, there have been only a handful of reports ofColletotrichumspp. isolated from aquatic plant hosts and their ecological role in the marine ecosystem is underexplored. To address this, we present the draft genome and annotation ofColletotrichumsp. CLE4, previously isolated from rhizome tissue from the seagrassZostera marina. This genome (48.03 Mbp in length) is highly complete (BUSCO ascomycota: 98.8%) and encodes 12,015 genes, of which 5.7% are carbohydrate-active enzymes (CAZymes) and 12.6% are predicted secreted proteins. Phylogenetic placement putsColletotrichumsp. CLE4 within theC. acutatumcomplex, closely related toC. godetiae. We found a 8.69% smaller genome size, 21.90% smaller gene count, and the absence of 591 conserved gene families inColletotrichumsp. CLE4 relative to other members of theC. acutatumcomplex, suggesting a streamlined genome possibly linked to its specialized ecological niche in the marine ecosystem. Machine learning analyses using CATAStrophy on CAZyme domains predict this isolate to be a hemibiotroph, such that it has a biotrophic phase where the plant is kept alive during optimal environmental conditions followed by a necrotrophic phase where the fungi actively serves a pathogen. While future work is still needed to definitively tease apart the lifestyle strategy ofColletotrichumsp. CLE4, this study provides foundational insight and a high-quality genomic resource for starting to understand the evolutionary trajectory and ecological adaptations of marine-plant associated fungi. 

ABSTRACT The glassy-winged sharpshooter,Homalodisca vitripennisGermar, is an invasive xylem-feeding leafhopper with a devastating economic impact on California agriculture through transmission of the plant pathogen,Xylella fastidiosa. While studies have focused onX. fastidiosaor known symbionts ofH. vitripennis, little work has been done at the scale of the microbiome (the bacterial community) or mycobiome (the fungal community). Here, we characterize the mycobiome and the microbiome ofH. vitripennisacross Southern California and explore correlations with captivity and host insecticide resistance status. Using high-throughput sequencing of the ribosomal internal transcribed spacer 1 region and the 16S rRNA gene to profile the mycobiome and microbiome, respectively, we found that while theH. vitripennismycobiome significantly varied across Southern California, the microbiome did not. We also observed a significant difference in both the mycobiome and microbiome between captive and wildH. vitripennis. Finally, we found that the mycobiome, but not the microbiome, was correlated with insecticide resistance status in wildH. vitripennis. This study serves as a foundational look at theH. vitripennismycobiome and microbiome across Southern California. Future work should explore the putative link between microbes and insecticide resistance status and investigate whether microbial communities should be considered inH. vitripennismanagement practices. IMPORTANCEThe glassy-winged sharpshooter is an invasive leafhopper that feeds on the xylem of plants and transmits the devastating pathogen,Xylella fastidiosa, resulting in significant economic damage to California’s agricultural system. While studies have focused on this pathogen or obligate symbionts of the glassy-winged sharpshooter, there is limited knowledge of the bacterial and fungal communities that make up its microbiome and mycobiome. To address this knowledge gap, we explored the composition of the mycobiome and the microbiome of the glassy-winged sharpshooter across Southern California and identified differences associated with geography, captivity, and host insecticide resistance status. Understanding sources of variation in the microbial communities associated with the glassy-winged sharpshooter is an important consideration for developing management strategies to control this invasive insect. This study is a first step toward understanding the role microbes may play in the glassy-winged sharpshooter’s resistance to insecticides. 

ABSTRACT We report six metagenome-assembled genomes (MAGs) associated with Massospora cicadina strain MCPNR19 (ARSEF 14555), an obligate entomopathogenic fungus of periodical cicadas. The MAGs include representatives of Pantoea , Pseudomonas , Lactococcus , and one potential new Chryseobacterium species. Future research is needed to resolve the ecology of these MAGs and determine whether they represent symbionts or contaminants. 

ABSTRACT A 1.488-Gb draft genome sequence was assembled for the fungus Massospora cicadina , an obligate parasite of periodical cicadas. The M. cicadina genome has experienced massive expansion via transposable elements (TEs), which account for 92% of the genome. 

Abstract BackgroundRock-dwelling microorganisms are key players in ecosystem functioning of Antarctic ice free-areas. Yet, little is known about their diversity and ecology, and further still, viruses in these communities have been largely unexplored despite important roles related to host metabolism and nutrient cycling. To begin to address this, we present a large-scale viral catalog from Antarctic rock microbial communities. ResultsWe performed metagenomic analyses on rocks from across Antarctica representing a broad range of environmental and spatial conditions, and which resulted in a predicted viral catalog comprising > 75,000 viral operational taxonomic units (vOTUS). We found largely undescribed, highly diverse and spatially structured virus communities which had predicted auxiliary metabolic genes (AMGs) with functions indicating that they may be potentially influencing bacterial adaptation and biogeochemistry. ConclusionThis catalog lays the foundation for expanding knowledge of virosphere diversity, function, spatial ecology, and dynamics in extreme environments. This work serves as a step towards exploring adaptability of microbial communities in the face of a changing climate. 

Abstract Background Homalodisca vitripennis Germar , the glassy-winged sharpshooter, is an invasive insect in California and a critical threat to agriculture through its transmission of the plant pathogen, Xylella fastidiosa . Quarantine, broad-spectrum insecticides, and biological control have been used for population management of H. vitripennis since its invasion and subsequent proliferation throughout California. Recently wide-spread neonicotinoid resistance has been detected in populations of H. vitripennis in the southern portions of California’s Central Valley. In order to better understand potential mechanisms of H. vitripennis neonicotinoid resistance, we performed RNA sequencing on wild-caught insecticide-resistant and relatively susceptible sharpshooters to profile their transcriptome and population structure. Results We identified 81 differentially expressed genes with higher expression in resistant individuals. The significant largest differentially expressed candidate gene linked to resistance status was a cytochrome P450 gene with similarity to CYP6A9. Furthermore, we observed an over-enrichment of GO terms representing functions supportive of roles in resistance mechanisms (cytochrome P450s, M13 peptidases, and cuticle structural proteins). Finally, we saw no evidence of broad-scale population structure, perhaps due to H. vitripennis' relatively recent introduction to California or due to the relatively small geographic scale investigated here. Conclusions In this work, we characterized the transcriptome of insecticide-resistant and susceptible H. vitripennis and identified candidate genes that may be involved in resistance mechanisms for this species. Future work should seek to build on the transcriptome profiling performed here to confirm the role of the identified genes, particularly the cytochrome P450, in resistance in H. vitripennis . We hope this work helps aid future population management strategies for this and other species with growing insecticide resistance.