Protein family content uncovers lineage relationships and bacterial pathway maintenance mechanisms in DPANN archaea

AbstractDPANN are small-celled archaea that are generally predicted to be symbionts, and in some cases are known episymbionts of other archaea. As the monophyly of the DPANN remains uncertain, we hypothesized that proteome content could reveal relationships among DPANN lineages, constrain genetic overlap with bacteria, and illustrate how organisms with hybrid bacterial and archaeal protein sets might function. We tested this hypothesis using protein family content that was defined in part using 569 newly reconstructed genomes. Protein family content clearly separates DPANN from other archaea, paralleling the separation of Candidate Phyla Radiation (CPR) bacteria from all other bacteria. This separation is partly driven by hypothetical proteins, some of which may be symbiosis-related. Pacearchaeota with the most limited predicted metabolic capacities have Form II/III and III-like Rubisco, suggesting metabolisms based on scavenged nucleotides. Intriguingly, the Pacearchaeota and Woesearchaeota with the smallest genomes also tend to encode large extracellular murein-like lytic transglycosylase domain proteins that may bind and degrade components of bacterial cell walls, indicating that some might be episymbionts of bacteria. The pathway for biosynthesis of bacterial isoprenoids is widespread in Woesearchaeota genomes and is encoded in proximity to genes involved in bacterial fatty acids synthesis. Surprisingly, in some DPANN genomes we identified a pathway for synthesis of queuosine, an unusual nucleotide in tRNAs of bacteria. Other bacterial systems are predicted to be involved in protein refolding. For example, many DPANN have the complete bacterial DnaK-DnaJ-GrpE system and many Woesearchaeota and Pacearchaeota possess bacterial group I chaperones. Thus, many DPANN appear to have mechanisms to ensure efficient protein folding of both archaeal and laterally acquired bacterial proteins.

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Protein Family Content Uncovers Lineage Relationships and Bacterial Pathway Maintenance Mechanisms in DPANN Archaea

Frontiers in Microbiology ◽

10.3389/fmicb.2021.660052 ◽

2021 ◽

Vol 12 ◽

Author(s):

Cindy J. Castelle ◽

Raphaël Méheust ◽

Alexander L. Jaffe ◽

Kiley Seitz ◽

Xianzhe Gong ◽

...

Keyword(s):

Cell Walls ◽

Protein Family ◽

Hypothetical Proteins ◽

Bacterial Group ◽

Archaeal Protein ◽

Bacterial Proteins ◽

Lytic Transglycosylase ◽

Group I ◽

Genetic Overlap ◽

Candidate Phyla Radiation

DPANN are small-celled archaea that are generally predicted to be symbionts, and in some cases are known episymbionts of other archaea. As the monophyly of the DPANN remains uncertain, we hypothesized that proteome content could reveal relationships among DPANN lineages, constrain genetic overlap with bacteria, and illustrate how organisms with hybrid bacterial and archaeal protein sets might function. We tested this hypothesis using protein family content that was defined in part using 3,197 genomes including 569 newly reconstructed genomes. Protein family content clearly separates the final set of 390 DPANN genomes from other archaea, paralleling the separation of Candidate Phyla Radiation (CPR) bacteria from all other bacteria. This separation is partly driven by hypothetical proteins, some of which may be symbiosis-related. Pacearchaeota with the most limited predicted metabolic capacities have Form II/III and III-like Rubisco, suggesting metabolisms based on scavenged nucleotides. Intriguingly, the Pacearchaeota and Woesearchaeota with the smallest genomes also tend to encode large extracellular murein-like lytic transglycosylase domain proteins that may bind and degrade components of bacterial cell walls, indicating that some might be episymbionts of bacteria. The pathway for biosynthesis of bacterial isoprenoids is widespread in Woesearchaeota genomes and is encoded in proximity to genes involved in bacterial fatty acids synthesis. Surprisingly, in some DPANN genomes we identified a pathway for synthesis of queuosine, an unusual nucleotide in tRNAs of bacteria. Other bacterial systems are predicted to be involved in protein refolding. For example, many DPANN have the complete bacterial DnaK-DnaJ-GrpE system and many Woesearchaeota and Pacearchaeota possess bacterial group I chaperones. Thus, many DPANN appear to have mechanisms to ensure efficient protein folding of both archaeal and laterally acquired bacterial proteins.

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The distinction of CPR bacteria from other bacteria based on protein family content

Nature Communications ◽

10.1038/s41467-019-12171-z ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 25

Author(s):

Raphaël Méheust ◽

David Burstein ◽

Cindy J. Castelle ◽

Jillian F. Banfield

Keyword(s):

Protein Family ◽

Cell Interactions ◽

Genome Reduction ◽

Protein Families ◽

Phylogenetic Structure ◽

Family Presence ◽

Core Sets ◽

Lineage Divergence ◽

Candidate Phyla Radiation ◽

Cell Cell

Abstract Candidate phyla radiation (CPR) bacteria separate phylogenetically from other bacteria, but the organismal distribution of their protein families remains unclear. Here, we leveraged sequences from thousands of uncultivated organisms and identified protein families that co-occur in genomes, thus are likely foundational for lineage capacities. Protein family presence/absence patterns cluster CPR bacteria together, and away from all other bacteria and archaea, partly due to proteins without recognizable homology to proteins in other bacteria. Some are likely involved in cell-cell interactions and potentially important for episymbiotic lifestyles. The diversity of protein family combinations in CPR may exceed that of all other bacteria. Over the bacterial tree, protein family presence/absence patterns broadly recapitulate phylogenetic structure, suggesting persistence of core sets of proteins since lineage divergence. The CPR could have arisen in an episode of dramatic but heterogeneous genome reduction or from a protogenote community and co-evolved with other bacteria.

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Bacterial group I introns: mobile RNA catalysts

Mobile DNA ◽

10.1186/1759-8753-5-8 ◽

2014 ◽

Vol 5 (1) ◽

pp. 8 ◽

Cited By ~ 36

Author(s):

Georg Hausner ◽

Mohamed Hafez ◽

David R Edgell

Keyword(s):

Group I Introns ◽

Bacterial Group ◽

Group I ◽

Rna Catalysts ◽

Mobile Rna

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A Kayvirus Distant Homolog of Staphylococcal Virulence Determinants and VISA Biomarker Is a Phage Lytic Enzyme

Viruses ◽

10.3390/v12030292 ◽

2020 ◽

Vol 12 (3) ◽

pp. 292

Author(s):

Aleksandra Głowacka-Rutkowska ◽

Magdalena Ulatowska ◽

Joanna Empel ◽

Magdalena Kowalczyk ◽

Jakub Boreczek ◽

...

Keyword(s):

Cell Walls ◽

Bacterial Transport ◽

Lytic Enzyme ◽

Virulence Determinants ◽

Gene Encoding ◽

Phage Gene ◽

E Coli ◽

Lytic Transglycosylase ◽

Distant Homolog

Staphylococcal bacteriophages of the Kayvirus genus are candidates for therapeutic applications. One of their proteins, Tgl, is slightly similar to two staphylococcal virulence factors, secreted autolysins of lytic transglycosylase motifs IsaA and SceD. We show that Tgl is a lytic enzyme secreted by the bacterial transport system and localizes to cell peripheries like IsaA and SceD. It causes lysis of E. coli cells expressing the cloned tgl gene, but could be overproduced when depleted of signal peptide. S. aureus cells producing Tgl lysed in the presence of nisin, which mimics the action of phage holin. In vitro, Tgl protein was able to destroy S. aureus cell walls. The production of Tgl decreased S. aureus tolerance to vancomycin, unlike the production of SceD, which is associated with decreased sensitivity to vancomycin. In the genomes of kayviruses, the tgl gene is located a few genes away from the lysK gene, encoding the major endolysin. While lysK is a late phage gene, tgl can be transcribed by a host RNA polymerase, like phage early genes. Taken together, our data indicate that tgl belongs to the kayvirus lytic module and encodes an additional endolysin that can act in concert with LysK in cell lysis.

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Assembly of core helices and rapid tertiary folding of a small bacterial group I ribozyme

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.0337743100 ◽

2003 ◽

Vol 100 (4) ◽

pp. 1574-1579 ◽

Cited By ~ 95

Author(s):

P. Rangan ◽

B. Masquida ◽

E. Westhof ◽

S. A. Woodson

Keyword(s):

Bacterial Group ◽

Group I ◽

Tertiary Folding

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Early acquisition of conserved, lineage-specific proteins currently lacking functional predictions were central to the rise and diversification of archaea

10.1101/2020.07.16.207365 ◽

2020 ◽

Author(s):

Raphaël Méheust ◽

Cindy J. Castelle ◽

Alexander L. Jaffe ◽

Jillian F. Banfield

Keyword(s):

Phylogenetic Tree ◽

Ammonia Oxidation ◽

Hypothetical Proteins ◽

Protein Families ◽

Eukaryotic Evolution ◽

Community Resource ◽

Archaeal Protein ◽

Genomic Analyses ◽

Specific Proteins ◽

Early Acquisition

AbstractRecent genomic analyses of Archaea have profoundly reshaped our understanding of their distribution, functionalities and roles in eukaryotic evolution. Within the domain, major supergroups are Euryarchaeota, which includes many methanogens, the TACK, which includes Thaumarchaeaota that impact ammonia oxidation in soils and the ocean, the Asgard, which includes lineages inferred to be ancestral to eukaryotes, and the DPANN, a group of mostly symbiotic small-celled archaea. Here, we investigated the extent to which clustering based on protein family content recapitulates archaeal phylogeny and identified the proteins that distinguish the major subdivisions. We also defined 10,866 archaeal protein families that will serve as a community resource. Clustering based on these families broadly recovers the archaeal phylogenetic tree. Interestingly, all major groups are distinguished primarily by the presence of families of conserved hypothetical proteins that are either novel or so highly diverged that their functions are obscured. Given that these hypothetical proteins are near ubiquitous within phyla, we conclude that they were important in the origin of most of the major archaeal lineages.

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Deep Annotation of Protein Function across Diverse Bacteria from Mutant Phenotypes

10.1101/072470 ◽

2016 ◽

Cited By ~ 21

Author(s):

Morgan N. Price ◽

Kelly M. Wetmore ◽

R. Jordan Waters ◽

Mark Callaghan ◽

Jayashree Ray ◽

...

Keyword(s):

Protein Function ◽

Large Scale ◽

Hypothetical Proteins ◽

Data Set ◽

Protein Coding ◽

Bacterial Proteins ◽

Genome Wide ◽

Protein Functions ◽

Mutant Phenotypes ◽

Related Proteins

SummaryThe function of nearly half of all protein-coding genes identified in bacterial genomes remains unknown. To systematically explore the functions of these proteins, we generated saturated transposon mutant libraries from 25 diverse bacteria and we assayed mutant phenotypes across hundreds of distinct conditions. From 3,903 genome-wide mutant fitness assays, we obtained 14.9 million gene phenotype measurements and we identified a mutant phenotype for 8,487 proteins with previously unknown functions. The majority of these hypothetical proteins (57%) had phenotypes that were either specific to a few conditions or were similar to that of another gene, thus enabling us to make informed predictions of protein function. For 1,914 of these hypothetical proteins, the functional associations are conserved across related proteins from different bacteria, which confirms that these associations are genuine. This comprehensive catalogue of experimentally-annotated protein functions also enables the targeted exploration of specific biological processes. For example, sensitivity to a DNA-damaging agent revealed 28 known families of DNA repair proteins and 11 putative novel families. Across all sequenced bacteria, 14% of proteins that lack detailed annotations have an ortholog with a functional association in our data set. Our study demonstrates the utility and scalability of high-throughput genetics for large-scale annotation of bacterial proteins and provides a vast compendium of experimentally-determined protein functions across diverse bacteria.

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