Borgs are giant extrachromosomal elements with the potential to augment methane oxidation
Preprint posted on 10 July 2021 https://www.biorxiv.org/content/10.1101/2021.07.10.451761v1.full
Categories: biochemistry, cell biology, evolutionary biology, genetics, genomics, molecular biology
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: 13 August 2021
doi: https://doi.org/10.1242/prelights.30205
Read preprint
(No Ratings Yet)Have your say
Sign up to customise the site to your preferences and to receive alerts
Register hereAlso in the biochemistry category:
Also in the cell biology category:
An epigenetic barrier sets the timing of human neuronal maturation
| Selected by | PiCLS Dundee |
1
mTORC1 is required for differentiation of germline stem cells in the Drosophila melanogaster testis
| Selected by | Diego Sainz de la Maza |
1
Expansion microscopy at one nanometer resolution
| Selected by | Nadja Hümpfer |
1
Also in the evolutionary biology category:
Epistasis between promoter activity and coding mutations shapes gene evolvability
| Selected by | Jennifer Ann Black |
1
The ELT-3 GATA factor specifies endoderm in Caenorhabditis angaria in an ancestral gene network
| Selected by | Chee Kiang Ewe |
3
Combinatorial interactions of Hox genes establish appendage diversity of the amphipod crustacean Parhyale hawaiensis
AND
Distinct regulation of Hox genes by Polycomb Group genes in a crustacean
| Selected by | Olivia Tidswell |
2
Also in the genetics category:
An epigenetic barrier sets the timing of human neuronal maturation
| Selected by | PiCLS Dundee |
1
mTORC1 is required for differentiation of germline stem cells in the Drosophila melanogaster testis
| Selected by | Diego Sainz de la Maza |
1
Dissecting aneuploidy phenotypes by constructing Sc2.0 chromosome VII and SCRaMbLEing synthetic disomic yeast
| Selected by | Grace Heredge Thomas |
Also in the genomics category:
Disrupting cellular memory to overcome drug resistance
| Selected by | Nate Mullin |
1
Comparative developmental genomics of sex-biased gene expression in early embryogenesis across mammals
| Selected by | Carly Guiltinan |
1
Telomere-to-telomere human DNA replication timing profiles
| Selected by | Jennifer Ann Black |
Also in the molecular biology category:
ARHGEF18 participates in Endothelial Cell Mechano-sensitivity in Response to Flow
| Selected by | Aarren Mannion |
Targeting a broad spectrum of KRAS-mutant cancers by hyperactivation-induced cell death
| Selected by | Yvonne Xinyi Lim |
1
Disrupting cellular memory to overcome drug resistance
| Selected by | Nate Mullin |
1
preLists in the biochemistry category:
20th “Genetics Workshops in Hungary”, Szeged (25th, September)
In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf
| List by | Nándor Lipták |
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
| List by | Osvaldo Contreras |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
| List by | Dey Lab |
Cellular metabolism
A curated list of preprints related to cellular metabolism at Biorxiv by Pablo Ranea Robles from the Prelights community. Special interest on lipid metabolism, peroxisomes and mitochondria.
| List by | Pablo Ranea Robles |
MitoList
This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.
| List by | Sandra Franco Iborra |
Also in the cell biology category:
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
| List by | Osvaldo Contreras |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
| List by | Ana Dorrego-Rivas |
BioMalPar XVI: Biology and Pathology of the Malaria Parasite
[under construction] Preprints presented at the (fully virtual) EMBL BioMalPar XVI, 17-18 May 2020 #emblmalaria
| List by | Dey Lab, Samantha Seah |
1
Cell Polarity
Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.
| List by | Yamini Ravichandran |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
3D Gastruloids
A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.
| List by | Paul Gerald L. Sanchez and Stefano Vianello |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
| List by | Dey Lab |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
| List by | Sandra Malmgren Hill |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
| List by | Rob Hynds |
Cellular metabolism
A curated list of preprints related to cellular metabolism at Biorxiv by Pablo Ranea Robles from the Prelights community. Special interest on lipid metabolism, peroxisomes and mitochondria.
| List by | Pablo Ranea Robles |
BSCB/BSDB Annual Meeting 2019
Preprints presented at the BSCB/BSDB Annual Meeting 2019
| List by | Dey Lab |
Biophysical Society Annual Meeting 2019
Few of the preprints that were discussed in the recent BPS annual meeting at Baltimore, USA
| List by | Joseph Jose Thottacherry |
ASCB/EMBO Annual Meeting 2018
This list relates to preprints that were discussed at the recent ASCB conference.
| List by | Dey Lab, Amanda Haage |
Also in the evolutionary biology category:
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
| List by | Ana Dorrego-Rivas |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
COVID-19 / SARS-CoV-2 preprints
List of important preprints dealing with the ongoing coronavirus outbreak. See http://covidpreprints.com for additional resources and timeline, and https://connect.biorxiv.org/relate/content/181 for full list of bioRxiv and medRxiv preprints on this topic
| List by | Dey Lab, Zhang-He Goh |
1
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
| List by | Alex Eve |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
| List by | Alexa Sadier |
Also in the genetics category:
Semmelweis Symposium 2022: 40th anniversary of international medical education at Semmelweis University
This preList contains preprints discussed during the 'Semmelweis Symposium 2022' (7-9 November), organised around the 40th anniversary of international medical education at Semmelweis University covering a wide range of topics.
| List by | Nándor Lipták |
20th “Genetics Workshops in Hungary”, Szeged (25th, September)
In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf
| List by | Nándor Lipták |
2nd Conference of the Visegrád Group Society for Developmental Biology
Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)
| List by | Nándor Lipták |
EMBL Conference: From functional genomics to systems biology
Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020
| List by | Jesus Victorino |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
| List by | Sandra Malmgren Hill |
Zebrafish immunology
A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.
| List by | Shikha Nayar |
Also in the genomics category:
Semmelweis Symposium 2022: 40th anniversary of international medical education at Semmelweis University
This preList contains preprints discussed during the 'Semmelweis Symposium 2022' (7-9 November), organised around the 40th anniversary of international medical education at Semmelweis University covering a wide range of topics.
| List by | Nándor Lipták |
20th “Genetics Workshops in Hungary”, Szeged (25th, September)
In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf
| List by | Nándor Lipták |
EMBL Conference: From functional genomics to systems biology
Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020
| List by | Jesus Victorino |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
Also in the molecular biology category:
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
| List by | Rob Hynds |
MitoList
This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.
| List by | Sandra Franco Iborra |
4 weeks
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.