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Borgs are giant extrachromosomal elements with the potential to augment methane oxidation

Basem Al-Shayeb, Marie C. Schoelmerich, Jacob West-Roberts, Luis E. Valentin-Alvarado, Rohan Sachdeva, Susan Mullen, Alexander Crits-Christoph, Michael J. Wilkins, Kenneth H. Williams, Jennifer A. Doudna, Jillian F. Banfield

Preprint posted on 10 July 2021 https://www.biorxiv.org/content/10.1101/2021.07.10.451761v1.full

Beware the Borg! Linear extrachromosomal DNA assimilated from Archaea

Selected by Kerryn Elliott

Updated 3 November 2022 with a postLight by Kerryn Elliott

This preprint was published in Nature on 27 October 2022, taking the coveted cover position! Congratulations to the authors! https://www.nature.com/nature/volumes/610/issues/7933

Overall, the paper remained essentially the same between the preprint and the published version. However, one of the clearest changes between the preprint and the published version was the sharpening of the title from “Borgs are giant extrachromosomal elements with the potential to augment methane oxidation” (specific) to “Borgs are giant genetic elements with the potential to expand metabolic capacity” a more general phenomenon.

Interestingly, the only change to the figures was to include an analysis of the abundance of specific Borgs and their correlation with certain methanoperedens species. This analysis found that there was an important correlation between species and the Borgs that were prevalent and that in some cases Borg DNA outnumbered genomic DNA 8:1. The remaining alterations were limited to the extended data, where a more thorough analysis of the relationship between the Borgs and other known linear bacterial plasmids did not find too many similarities, giving further support to Borgs being unlike anything seen before.

Finally, one of my queries to the authors was what would be required to classify the Borgs as viruses, plasmids or mini-chromosomes, and although they were unable to find any evidence to classify them as one or the other, they did include an additional sentence to suggest they could be classified as “megaplasmids”, a completely novel entity.

Background

Methane is the second most abundant greenhouse gas after carbon dioxide, and although it is comparatively short lived in the atmosphere, methane is almost 30 times more potent at warming the earth than carbon dioxide. Methane is produced by microbiological processes, and one gigaton of methane is produced annually by methanogenic (methane-producing) archaea. Methanotrophs, on the other hand, are methane-oxidising microorganisms with the ability to reduce methane levels in the atmosphere, and therefore limit global warming. One such methanotroph is an anaerobic methanotrophic archaea (ANME) known as Methanoperedens, which is capable of directly coupling methane oxidation to the reduction of iron, nitrate or manganese.

Previous work has shown that different factors can impact the rate of methane oxidation. In order to investigate the factors, such as viruses, which have been suggested to influence the methane oxidation rate of Methanoperedens, the authors sampled soil from wetlands in California where methane oxidation and Methanoperedens are known to occur.  In this preprint, they report the identification of novel extrachromosomal elements, which they term ‘Borgs’ with the ability to augment the methane oxidation capacity of Methanoperedens. They hypothesise that Borgs have a potential role in the mitigation of greenhouse gas emissions in the future.

Main findings

The authors first sampled the soils from a number of saturated vernal pools (wetland) locations in California, and performed Illumina sequencing on the bulk environmental DNA extracted from both these samples and sediment samples from an aquifer in Colorado. A variety of tools were used to assemble the sequences into de novo sequences which were then compared to the existing databases UniProt and ggKbase to determine the taxonomy. Hundreds of kilobases of assembled sequences (contigs) were flagged as extrachromosomal elements as they did not fit any taxonomy at the domain level (Bacteria, Archaea, Eukaryotes).

The authors manually curated these large contigs to generate four complete genomes, as well as an additional partial genome. The four genomes ranged in size from 661,708 to 918,293 kbp and all contained a large inverted repeat (about 1.5 kbp) at the end of the linear genome, as well as interspersed regions of tandem repeats throughout the genomes. All genomes consisted of two replicores, which were unequal in length and carried all genes on one strand. Although the majority of the identified genes were novel, 21% of the predicted proteins had database matches, and the majority of those had a best match to Methanoperedens. Interestingly, although they had a 10% lower GC content than previously existing species, there were certain gene cluster regions that had clear increases in GC content up to the expected GC of Methanoperedens species, which also displayed much greater similarity at the protein sequence level to Methanoperedens, suggesting that these pieces of DNA had been acquired by lateral gene transfer from Methanoperedens. The genomes lacked key ribosomal and other single-copy genes required for Archaea life, and therefore represented a novel extrachromosomal element, which the authors termed “Borgs” due to their ability to assimilate genes from organisms, such as Methanoperedens.

Using the manually curated genomes the authors then compiled criteria to search for additional Borg genomes, and detected a total of 19 different Borg genomes in their samples. There were more Borg sequences found in deeper soil, and there was no clear relationship between the abundance of coexisting Methanoperedens species, with Borgs being detected up to 8x more frequently than the Archaea, confirming that Borg genomes also shared regions of similarity throughout their genomes, and indeed there was one pair which shared 100 % nucleotide identity for an 11 kb region, suggesting a recent combination event.

What do the Borgs encode?

The Borg genomes contained a variety of proteins, and the majority of them have unknown function. All Borg genomes encoded the ribosomal protein rpL11, and some contained other ribosomal proteins. Many Borg genomes encoded mobile element defense systems, including RNA-targeting type III-A CRISPR-Cas systems. The most represented functions for the encoded Borg proteins were DNA or RNA manipulation, energy metabolism and Glycosyltransferases. Intriguingly, all Borgs contained FtsZ-tubulin homologs possibly involved in membrane remodeling or division. They also contain proteins that resemble Major Vault Proteins and the TEP1-like TROVE domain protein, which together form a ribonucleoprotein known as the eukaryotic vault organelle, which may be involved in drug resistance.

The prevalence of a variety of genes with redox or respiratory functions also varied across different Borg genomes. The Black Borg encoded genes involved in methane oxidation, which appeared to be derived recently from Methanoperedens based on GC content. Eight Borgs encoded genes for the biosynthesis of tetrahydromethanopterin, a coenzyme used in methanogenesis, as well as ferredoxin proteins which could be the electron carriers. The Lilac Borg, which was unique in its association with a certain species of Methanoperedens, encoded the methyl-CoM reductase complex, which is central to methane processing. This complex in the Lilac Borg genome shares 75-88% amino acid sequence identity to the associated Methanoperedens genome. This complex is also encoded by the Steel borg. This is the first time methane metabolism genes have been detected on extrachomosomal elements and could represent a mechanism for dispersal of such elements. As with all Borgs, the Lilac Borg lacks the capacity for independent existence. The authors postulate that instead the Lilac Borg, lives within its host Methanoperedens cells, and may provide important metabolic genes to the host cells.

Conclusion

The extrachromosomal Borg elements represent something very different from anything that has been identified before. They are larger than other known Archaea viruses, and do not show similarity to anything that has been previously reported. Although they appear to have some association with Methanoperedens species, the exact connection to the Archaea is unclear. The fact that they carry metabolic genes, and could even regulate methane levels, giving the surrounding species an advantage and is very intriguing. More broadly speaking, Borgs have the potential to influence methane mitigation in the future, with implications for climate change. I look forward to future research into the role of the Borg.

Why I chose this paper

The entire concept is very intriguing! A giant extrachromosomal element which has the potential to influence metabolism? I had to learn more about it 🙂

I love the idea of basic research, that is collecting mud samples, leading to important findings for the future.

 

Questions to the Authors

Tell us a bit more about how you named them “Borg” and the inspiration for giving them colour names.

Can you explain a bit more about how  you compile a new chromosome from the environmental DNA? For example, how do you make new contigs from 150 to 250 bp reads? How much overlap is there? Are there multiple copies of these sequences which allows a new contig to be assembled with confidence?

Is it possible to use long read sequencing like nanopore or PacBio on the environmental DNA?

You state: “We can neither prove that they are archaeal viruses or plasmids or mini-chromosomes, nor can we prove that they are not” Why is this? What would be required to determine what they actually are?

 

Posted on: 12 August 2021 , updated on: 19 December 2022

doi: https://doi.org/10.1242/prelights.30205

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Author's response

Basem Al-Shayeb shared

Can you explain a bit more about how  you compile a new chromosome from the environmental DNA? For example, how do you make new contigs from 150 to 250 bp reads? How much overlap is there? Are there multiple copies of these sequences which allows a new contig to be assembled with confidence?

It is a combination of overlaps in sequencing reads, as well as sequencing coverage, overall GC content, tetranucleotide frequency, and other factors that should be consistent throughout a single genome.

Is it possible to use long read sequencing like nanopore or PacBio on the environmental DNA?

Yes

You state: “We can neither prove that they are archaeal viruses or plasmids or mini-chromosomes, nor can we prove that they are not” Why is this? What would be required to determine what they actually are?

We would need to see the structural proteins that make up a virus, or the replication and other proteins that constitute a megaplasmid or minichromosome.  Since we couldn’t identify anything that would suggest this, we can’t classify them as those classes, but at the same time the majority of genes are unknown so we can’t say they aren’t an extremely novel virus or plasmid

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