Attention:The NSF Public Access Repository (PAR) system and access will be unavailable from 5:00 PM ET until 8:00 PM ET on Friday, September 11 due to maintenance. We apologize for the inconvenience.


Title: Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires
Abstract Borgs are huge extrachromosomal elements (ECE) of anaerobic methane-consuming “CandidatusMethanoperedens” archaea. Here, we used nanopore sequencing to validate published complete genomes curated from short reads and to reconstruct new genomes. 13 complete and four near-complete linear genomes share 40 genes that define a largely syntenous genome backbone. We use these conserved genes to identify new Borgs from peatland soil and to delineate Borg phylogeny, revealing two major clades. Remarkably, Borg genes encoding nanowire-like electron-transferring cytochromes and cell surface proteins are more highly expressed than those of hostMethanoperedens, indicating that Borgs augment theMethanoperedensactivity in situ. We reconstructed the first complete 4.00 Mbp genome for aMethanoperedensthat is inferred to be a Borg host and predicted its methylation motifs, which differ from pervasive TC and CC methylation motifs of the Borgs. Thus, methylation may enableMethanoperedensto distinguish their genomes from those of Borgs. Very high Borg toMethanoperedensratios and structural predictions suggest that Borgs may be capable of encapsulation. The findings clearly define Borgs as a distinct class of ECE with shared genomic signatures, establish their diversification from a common ancestor with genetic inheritance, and raise the possibility of periodic existence outside of host cells.  more » « less
Award ID(s):
2210473
PAR ID:
10563562
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Nature Communications
Date Published:
Journal Name:
Nature Communications
Volume:
15
Issue:
1
ISSN:
2041-1723
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Hom, Erik_F Y (Ed.)
    ABSTRACT Viruses that infect phytoplankton are an integral part of marine ecosystems, but the vast majority of viral diversity remains uncultivated. Here, we introduce four near-complete genomic assemblies of viruses that infect the widespread marine picoeukaryoteMicromonas commoda, doubling the number of reported genomes ofMicromonasdsDNA viruses. All host and virus isolates were obtained from tropical waters of the North Pacific, a first for viruses infecting green algae in the order Mamiellales. Genome length of the new isolates ranges from 205 to 212 kb, and phylogenetic analysis shows that all four are members of the genusPrasinovirus. Three of the viruses form a clade that is adjacent to previously sequencedMicromonasviruses, while the fourth virus is relatively divergent from previously sequenced prasinoviruses. We identified 61 putative genes not previously found in prasinovirus isolates, including a phosphate transporter and a potential apoptosis inhibitor novel to marine viruses. Forty-eight genes in the new viruses are also found in host genome(s) and may have been acquired through horizontal gene transfer. By analyzing the coding sequences of all published prasinoviruses, we found that ~25% of prasinovirus gene content is significantly correlated with host genus identity (i.e.,Micromonas,Ostreococcus, orBathycoccus), and the functions of these genes suggest that much of the viral life cycle is differentially adapted to the three host genera. Mapping of metagenomic reads from global survey data indicates that one of the new isolates, McV-SA1, is relatively common in multiple ocean basins.IMPORTANCEThe genomes analyzed here represent the first viruses from the tropical North Pacific that infect the abundant phytoplankton order Mamiellales. Comparing isolates from the same location demonstrates high genomic diversity among viruses that co-occur and presumably compete for hosts. Comparing all published prasinovirus genomes highlights gene functions that are likely associated with adaptation to different host genera. Metagenomic data indicate these viruses are globally distributed, and one of the novel isolates may be among the most abundant marine viruses. 
    more » « less
  2. Abstract Diverse members of early-diverging Mucoromycota, including mycorrhizal taxa and soil-associated Mortierellaceae, are known to harbor Mollicutes-related endobacteria (MRE). It has been hypothesized that MRE were acquired by a common ancestor and transmitted vertically. Alternatively, MRE endosymbionts could have invaded after the divergence of Mucoromycota lineages and subsequently spread to new hosts horizontally. To better understand the evolutionary history of MRE symbionts, we generated and analyzed four complete MRE genomes from two Mortierellaceae genera:Linnemannia(MRE-L) andBenniella(MRE-B). These genomes include the smallest known of fungal endosymbionts and showed signals of a tight relationship with hosts including a reduced functional capacity and genes transferred from fungal hosts to MRE. Phylogenetic reconstruction including nine MRE from mycorrhizal fungi revealed that MRE-B genomes are more closely related to MRE from Glomeromycotina than MRE-L from the same host family. We posit that reductions in genome size, GC content, pseudogene content, and repeat content in MRE-L may reflect a longer-term relationship with their fungal hosts. These data indicateLinnemanniaandBenniellaMRE were likely acquired independently after their fungal hosts diverged from a common ancestor. This work expands upon foundational knowledge on minimal genomes and provides insights into the evolution of bacterial endosymbionts. 
    more » « less
  3. Abstract The symbiosis between clownfish and giant tropical sea anemones (Order Actiniaria) is one of the most iconic on the planet. Distributed on tropical reefs, 28 species of clownfishes form obligate mutualistic relationships with 10 nominal species of venomous sea anemones. Our understanding of the symbiosis is limited by the fact that most research has been focused on the clownfishes. Chromosome scale reference genomes are available for all clownfish species, yet there are no published reference genomes for the host sea anemones. Recent studies have shown that the clownfish-hosting sea anemones belong to three distinct clades of sea anemones that have evolved symbiosis with clownfishes independently. Here we present the first high quality long read assemblies for three species of clownfish hosting sea anemones belonging to each of these clades:Entacmaea quadricolor, Stichodactyla haddoni, Radianthus doreensis. PacBio HiFi sequencing yielded 1,597,562, 3,101,773, and 1,918,148 million reads forE. quadricolor, S. haddoni, andR. doreensis, respectively. All three assemblies were highly contiguous and complete with N50 values above 4Mb and BUSCO completeness above 95% on the Metazoa dataset. Genome structural annotation with BRAKER3 predicted 20,454, 18,948 and 17,056 protein coding genes inE. quadricolor, S. haddoniandR. doreeensisgenome, respectively. These new resources will form the basis of comparative genomic analyses that will allow us to deepen our understanding of this mutualism from the host perspective. SignificanceChromosome-scale genomes are available for all 28 clownfish species yet there are no high-quality reference genomes published for the clownfish-hosting sea anemones. The lack of genomic resources impedes our ability to understand evolution of this iconic symbiosis from the host perspective. The clownfish-hosting sea anemones belong to three clades of sea anemones that have evolved mutualism with clownfish independently. Here we assembled the first high-quality long-read genomes for three species of host sea anemones each belonging to a different host clade:Entacmaea quadricolor, Stichodactyla haddoni, Radianthus doreensis. These resources will enable in depth comparative genomics of clownfish-hosting sea anemones providing a critical perspective for understanding how the symbiosis has evolved. Finally, these reference genomes present a significant increase in the number of high-quality long-read genome assemblies for sea anemones (11 currently published) and double the number of high-quality reference genomes for the sea anemone superfamily Actinoidea. 
    more » « less
  4. Campbell, Barbara J (Ed.)
    ABSTRACT Seaweeds harbor a rich diversity of bacteria, providing them with metabolic resources and a surface for attachment and biofilm development. The host’s unique environment potentially shapes the bacterial genomes and promotes adaptations for a symbiotic lifestyle. To investigate whether the genomes of seaweed-associated bacteria are genetically and metabolically distinct from their close free-living relatives in seawater, we compared both the seaweed-associated and free-living counterparts of 72 bacterial genera across 16 seaweed hosts using whole-genome sequences or high-quality metagenome-assembled genomes. While taxonomic affiliation strongly influenced genome characteristics such as GC content, gene number, and size, host association had a lower effect overall. A reduced genome size was suggested only inNereocystis luetkeana-associated microbes, while onlyAscophyllum nodosum-associated bacteria had an increased GC content. Metabolic adaptations were indicated from the genomes of seaweed-associated bacteria, including enriched pathways for B vitamin production, complex carbohydrate utilization, and amino acid biosynthesis. In particular,Flavobacteriiashowed the most pronounced differences between host-associated and free-living strains. We further hypothesized that bacteria associated with seaweed might have evolved to complement their host’s metabolism and tested this inference by analyzing the genomes of both the seaweedEctocarpus subulatusand its 28 bacterial associates but found no evidence for such complementarity. Our analyses of 72 paired bacterial genomes highlighted significant metabolic differences in seaweed-associated strains with implications for carbon, nitrogen, and sulfur cycling in the coastal ocean. IMPORTANCEWe hypothesized that the unique environment of seaweeds in coastal oceans shapes bacterial genomes and promotes a symbiotic lifestyle. We compared the genomes of bacteria isolated from seaweed with bacteria from the same genus found free-living in seawater. For genome features that included the number of genes, the size of the genome, and the GC content, taxonomy was of greater importance than bacterial lifestyle. When we compared metabolic abilities, we again found a strong effect of taxonomy in determining metabolism. Although several metabolic pathways differed between free-living and host-associated bacteria, this was especially prominent forFlavobacteriiain the phylumBacteroidota. Notably, bacteria living on seaweeds had an increased occurrence of genes for B vitamin synthesis, complex carbohydrate use, and nitrogen uptake, indicating that bacterial genomes reflect both their evolutionary history and the current environment they inhabit. 
    more » « less
  5. Summary Polyploidy is an important evolutionary force, yet epigenetic mechanisms, such as DNA methylation, that regulate genome‐wide expression of duplicated genes remain largely unknown. Here, we useTragopogon(Asteraceae) as a model system to discover patterns and temporal dynamics of DNA methylation in recently formed polyploids.The naturally occurring allotetraploidTragopogon miscellusformed in the last 95–100 yr from parental diploidsTragopogon dubiusandT. pratensis. We profiled the DNA methylomes of these three species using whole‐genome bisulfite sequencing.Genome‐wide methylation levels inT. miscelluswere intermediate between its diploid parents. However, nonadditive CG and CHG methylation occurred in transposable elements (TEs), with variation among TE types. Most differentially methylated regions (DMRs) showed parental legacy, but some novel DMRs were detected in the polyploid. Differentially methylated genes (DMGs) were also identified and characterized.This study provides the first assessment of both overall and locus‐specific patterns of DNA methylation in a recent natural allopolyploid and shows that novel methylation variants can be generated rapidly after polyploid formation. Together, these results demonstrate that mechanisms to regulate duplicate gene expression may arise soon after allopolyploid formation and that these mechanisms vary among genes. 
    more » « less