Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea

Zhu, Quanyin; Mai, Uyen; Pfeiffer, Wayne; Janssen, Stefan; Asnicar, Francesco; Sanders, Jon G.; Belda-Ferre, Pedro; Al‐Ghalith, Gabriel A.; Kopylova, Evguenia; McDonald, Daniel; Kościółek, Tomasz; Yin, John B.; Huang, Shi; Salam, Nimaichand; Jiao, Jian Yu; Wu, Zhenru; Xu, Zhenjiang Zech; Cantrell, Kalen; Yang, Yimeng; Sayyari, Erfan; Rabiee, Maryam; Morton, James T.; Podell, Sheila; Knights, Dan; Li, Wen Jun; Huttenhower, Curtis; Segata, Nicola; Smarr, Larry; Mirarab, Siavash; Knight, Rob

doi:10.1038/s41467-019-13443-4

Cited by 275 publications

(402 citation statements)

References 91 publications

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“…3A-B , Table S1). This finding was validated in an independent dataset by mapping the Web of Life (WoL) microbial genomes (Zhu et al, 2019) to 16S rRNA gene amplicon sequence variants (ASVs) from over 20,000 samples in the American Gut Project (AGP), a citizen-science dataset with participants ranging in age from 1-80 years (McDonald et al, 2018). A similar age and sex-dependent decrease in HS-modifying bacteria was observed (Nstrains numerator = 244 & denominator = 1605) ( Fig.…”

Section: Bacteria With Capacity For Hs Modification Decrease With Agementioning

confidence: 54%

“…Demultiplexed shallow shotgun metagenomic sequences were quality filtered and adapter trimmed using Atropos (Didion et al, 2017), and human filtered using Bowtie2 (Langmead and Salzberg, 2012). For taxonomic assignment reads were aligned to the Web of Life database (Zhu et al, 2019) of 10,575 bacterial and archaeal genomes using Shogun (Hillmann et al, 2018) in the Bowtie2 alignment mode. For functional assignment of glycosylation-associated genes the FINRISK 2002 data were aligned to the HS degradation gene set of glycosylation-associated genes are using Bowtie2.…”

Section: Finriskmentioning

confidence: 99%

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Bacterial modification of the host glycosaminoglycan heparan sulfate modulates SARS-CoV-2 infectivity

Martino

Kellman

Sandoval

et al. 2020

Preprint

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The human microbiota has a close relationship with human disease and it remodels components of the glycocalyx including heparan sulfate (HS). Studies of the severe acute respiratory syndrome coronavirus (SARS-CoV-2) spike protein receptor binding domain suggest that infection requires binding to HS and angiotensin converting enzyme 2 (ACE2) in a codependent manner. Here, we show that commensal host bacterial communities can modify HS and thereby modulate SARS-CoV-2 spike protein binding and that these communities change with host age and sex. Common human-associated commensal bacteria whose genomes encode HS-modifying enzymes were identified. The prevalence of these bacteria and the expression of key microbial glycosidases in bronchoalveolar lavage fluid (BALF) was lower in adult COVID-19 patients than in healthy controls. The presence of HS-modifying bacteria decreased with age in two large survey datasets, FINRISK 2002 and American Gut, revealing one possible mechanism for the observed increase in COVID-19 susceptibility with age. In vitro, bacterial glycosidases from unpurified culture media supernatants fully blocked SARS-CoV-2 spike binding to human H1299 protein lung adenocarcinoma cells. HS-modifying bacteria in human microbial communities may regulate viral adhesion, and loss of these commensals could predispose individuals to infection. Understanding the impact of shifts in microbial community composition and bacterial lyases on SARS-CoV-2 infection may lead to new therapeutics and diagnosis of susceptibility.

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Section: Bacteria With Capacity For Hs Modification Decrease With Agementioning

confidence: 54%

Section: Finriskmentioning

confidence: 99%

Bacterial modification of the host glycosaminoglycan heparan sulfate modulates SARS-CoV-2 infectivity

Martino

Kellman

Sandoval

et al. 2020

Preprint

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“…Initially described as a radiation of phylum-level clades based on analyses of 16S rRNA divergence (Brown et al, 2015) , the CPR has been thought to comprise at least 15% of bacterial phylum-level groups (Brown et al, 2015) , potentially matching the scale of all other bacterial diversity . Attempts to adjust for lineage specific evolutionary rates have suggested the collapse of CPR into a single phylum (Parks et al, 2018) , but more recent analyses with balanced taxonomic sampling continue to depict it as a substantial component of the bacterial domain (Zhu et al 2019). Here, we combined new and previously reported genomes to construct a robust tree for the CPR radiation using two unlinked, concatenated marker sets (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…The Candidate Phyla Radiation, a large group of bacterial lineages lacking pure isolate cultures, are one group primarily defined through genome-resolved metagenomics (Brown et al, 2015;Luef et al, 2015) . While estimates vary depending on the methods used Parks et al, 2018) , CPR are predicted to constitute a significant portion of bacterial diversity that is distinct and divergent from other bacterial groups (Zhu et al, 2019) . Additionally, CPR bacteria generally have relatively small genome and cell sizes, extremely reduced genomic repertoires, and often lack the capacity to synthesize lipids (Brown et al, 2015;Kantor et al, 2013;Luef et al, 2015) .…”

Section: Introductionmentioning

confidence: 99%

The rise of diversity in metabolic platforms across the Candidate Phyla Radiation

Jaffe

Castelle

Carnevali

et al. 2019

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A unifying feature of the bacterial Candidate Phyla Radiation (CPR) is a limited and highly variable repertoire of biosynthetic capabilities. However, the distribution of metabolic traits across the CPR and the evolutionary processes underlying them are incompletely resolved. Here, we selected~1,000 genomes of CPR bacteria from diverse environments to construct a robust internal phylogeny that was consistent across two unlinked marker sets. Mapping of glycolysis, the pentose phosphate pathway, and pyruvate metabolism onto the tree showed that some components of these pathways are sparsely distributed and that similarity between metabolic platforms is only partially predicted by phylogenetic relationships. To evaluate the extent to which gene loss and lateral gene transfer have shaped trait distribution , we analyzed the patchiness of gene presence in a phylogenetic context, examined the phylogenetic depth of clades with shared traits, and compared the reference tree topology with those of specific metabolic proteins. While the central glycolytic pathway in CPR is widely conserved and has likely been shaped primarily by vertical transmission, there is evidence for both gene loss and transfer especially in steps that convert glucose into fructose 1,6-bisphosphate and glycerate 3P into pyruvate. Additionally, the distribution of Group 3 and Group 4-related NiFe hydrogenases is patchy and suggests multiple events of ancient gene transfer. Overall, patterns of gene gain and loss, including acquisition of accessory traits in independent transfer events, may have been driven by shifts in host-derived resources and led to sparse but varied genetic inventories. INTRODUCTION :

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“…Thus, we argue that many MTB-containing lineages await discovery. Future discovery of additional MTB affiliated within other Bacterial phyla, especially those near the base of the Bacterial tree 81,82 , will help to understand and constrain the evolutionary origin of the magnetosome organelle.…”

Section: Resultsmentioning

confidence: 99%

Expanding magnetic organelle biogenesis in the domainBacteria

Lin

Zhang

Paterson

et al. 2020

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21The discovery of membrane-enclosed, metabolically functional organelles in 22 Bacteria and Archaea has transformed our understanding of the subcellular 23 complexity of prokaryotic cells. However, whether prokaryotic organelles 24 emerged early or late in evolutionary history remains unclear and limits 25 understanding of the nature and cellular complexity of early life. 26 Biomineralization of magnetic nanoparticles within magnetosomes by 27 magnetotactic bacteria (MTB) is a fascinating example of prokaryotic organelles. 28 Here, we reconstruct 168 metagenome-assembled MTB genomes from various 29 aquatic environments and waterlogged soils. These genomes represent nearly a 3-30 fold increase over the number currently available, and more than double the 31 known MTB species. Phylogenomic analysis reveals that these newly described 32 genomes belong to 13 Bacterial phyla, six of which were previously not known to 33 include MTB. These findings indicate a much wider taxonomic distribution of 34 magnetosome organelle biogenesis across the domain Bacteria than previously 35 thought. Comparative genome analysis reveals a vast diversity of magnetosome 36 gene clusters involved in magnetosomal biogenesis in terms of gene content and 37 synteny residing in distinct taxonomic lineages. These gene clusters therefore 38 represent a promising, diverse genetic resource for biosynthesizing novel magnetic 39 nanoparticles. Finally, our phylogenetic analyses of the core magnetosome 40 proteins in this largest available and taxonomically diverse dataset support an 41 unexpectedly early evolutionary origin of magnetosome biomineralization, likely 42 ancestral to the origin of the domain Bacteria. These findings emphasize the 43 potential biological significance of prokaryotic organelles on the early Earth and 44 have important implications for our understanding of the evolutionary history of 45 cellular complexity.46 47It was accepted widely that intracellular, membrane-bounded, metabolically functional 48 organelles are present exclusively in eukaryotic cells and that they are absent from 49 Bacteria and Archaea. This long-held view was revised after numerous recent 50 discoveries of a diverse group of highly organized, membrane-enclosed organelles in 51 the domains Bacteria and Archaea associated with specific cellular functions 1-3 . 52However, the origin and evolution of prokaryotic organelles remain largely elusive. It 53 is still unclear whether organelle biogenesis emerged early or late during the evolution 54 of Bacteria and Archaea, posing problems for elucidating the evolutionary history of 55 cellular complexity. 56 Magnetosomes within magnetotactic bacteria (MTB) are a striking example of 57 prokaryotic organelles 4 . Magnetosomes consist of a lipid bilayer-bounded membrane 58 in which nanosized, ferrimagnetic magnetite (Fe3O4) and/or greigite (Fe3S4) crystals 59 are biomineralized and usually arranged in chain-like structure(s) that maximize the 60 magnetic dipole moment 5,6 (Figure 1). The most accepted maj...

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Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea

Cited by 275 publications

References 91 publications

Bacterial modification of the host glycosaminoglycan heparan sulfate modulates SARS-CoV-2 infectivity

Bacterial modification of the host glycosaminoglycan heparan sulfate modulates SARS-CoV-2 infectivity

The rise of diversity in metabolic platforms across the Candidate Phyla Radiation

Expanding magnetic organelle biogenesis in the domainBacteria

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