Conservative route to genome compaction in a miniature annelid

SummaryThe causes and consequences of genome reduction in animals are unclear, because our understanding of this process mostly relies on lineages with often exceptionally high rates of evolution. Here, we decode the compact 73.8 Mb genome of Dimorphilus gyrociliatus, a meiobenthic segmented worm. The D. gyrociliatus genome retains traits classically associated with larger and slower-evolving genomes, such as an ordered, intact Hox cluster, a generally conserved developmental toolkit, and traces of ancestral bilaterian linkage. Unlike some other animals with small genomes, the analysis of the D. gyrociliatus epigenome revealed canonical features of genome regulation, excluding the presence of operons and trans-splicing. Instead, the gene dense D. gyrociliatus genome presents a divergent Myc pathway, a key physiological regulator of growth, proliferation, and genome stability in animals. Altogether, our results uncover a conservative route to genome compaction in annelids, reminiscent of that observed in the vertebrate Takifugu rubripes.

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Conservative route to genome compaction in a miniature annelid

Nature Ecology & Evolution ◽

10.1038/s41559-020-01327-6 ◽

2020 ◽

Author(s):

José M. Martín-Durán ◽

Bruno C. Vellutini ◽

Ferdinand Marlétaz ◽

Viviana Cetrangolo ◽

Nevena Cvetesic ◽

...

Keyword(s):

Genome Stability ◽

Genome Reduction ◽

Takifugu Rubripes ◽

Hox Cluster ◽

Genome Regulation ◽

Rates Of Evolution ◽

Physiological Regulator ◽

Cluster A

AbstractThe causes and consequences of genome reduction in animals are unclear because our understanding of this process mostly relies on lineages with often exceptionally high rates of evolution. Here, we decode the compact 73.8-megabase genome of Dimorphilus gyrociliatus, a meiobenthic segmented worm. The D. gyrociliatus genome retains traits classically associated with larger and slower-evolving genomes, such as an ordered, intact Hox cluster, a generally conserved developmental toolkit and traces of ancestral bilaterian linkage. Unlike some other animals with small genomes, the analysis of the D. gyrociliatus epigenome revealed canonical features of genome regulation, excluding the presence of operons and trans-splicing. Instead, the gene-dense D. gyrociliatus genome presents a divergent Myc pathway, a key physiological regulator of growth, proliferation and genome stability in animals. Altogether, our results uncover a conservative route to genome compaction in annelids, reminiscent of that observed in the vertebrate Takifugu rubripes.

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Chlamydiapan-genomic analysis reveals balance between host adaptation and selective pressure to genome reduction

10.1101/506121 ◽

2018 ◽

Cited By ~ 1

Author(s):

Olga Sigalova ◽

Andrei V Chaplin ◽

Olga O Bochkareva ◽

Pavel Shelyakin ◽

Vsevolod A Filaretov ◽

...

Keyword(s):

Genome Stability ◽

Selective Pressure ◽

Large Fraction ◽

Genomic Analysis ◽

Gene Families ◽

Genome Reduction ◽

Host Immune System ◽

Parasitic Lifestyle ◽

Genomic Locations ◽

Conserved Core

AbstractChlamydiaare ancient intracellular pathogens with reduced, though strikingly conserved genome. Despite their parasitic lifestyle and isolated intracellular environment, these bacteria managed to avoid accumulation of deleterious mutations leading to subsequent genome degradation characteristic for many parasitic bacteria.We report pan-genomic analysis of eleven species from genusChlamydiaincluding identification and functional annotation of orthologous genes, and characterization of gene gains, losses, and rearrangements. We demonstrate the overall genome stability of these bacteria as indicated by a large fraction of common genes with conserved genomic locations. On the other hand, extreme evolvability is confined to several paralogous gene families such as polymorphic membrane proteins and phospholipase D and likely is caused by the pressure from the host immune system.This combination of a large, conserved core genome and a small, evolvable periphery likely reflect the balance between the selective pressure towards genome reduction and the need to adapt to changing host environment.

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The mouse alpha-globin cluster: a paradigm for studying genome regulation and organization

Current Opinion in Genetics & Development ◽

10.1016/j.gde.2020.10.003 ◽

2021 ◽

Vol 67 ◽

pp. 18-24

Author(s):

A Marieke Oudelaar ◽

Robert A Beagrie ◽

Mira T Kassouf ◽

Douglas R Higgs

Keyword(s):

Genome Regulation ◽

Alpha Globin ◽

Cluster A

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Chlamydia pan-genomic analysis reveals balance between host adaptation and selective pressure to genome reduction

BMC Genomics ◽

10.1186/s12864-019-6059-5 ◽

2019 ◽

Vol 20 (1) ◽

Cited By ~ 1

Author(s):

Olga M. Sigalova ◽

Andrei V. Chaplin ◽

Olga O. Bochkareva ◽

Pavel V. Shelyakin ◽

Vsevolod A. Filaretov ◽

...

Keyword(s):

Genome Stability ◽

Selective Pressure ◽

Large Fraction ◽

Genomic Analysis ◽

Gene Families ◽

Genome Reduction ◽

Host Immune System ◽

Parasitic Lifestyle ◽

Genomic Locations ◽

Conserved Core

Abstract Background Chlamydia are ancient intracellular pathogens with reduced, though strikingly conserved genome. Despite their parasitic lifestyle and isolated intracellular environment, these bacteria managed to avoid accumulation of deleterious mutations leading to subsequent genome degradation characteristic for many parasitic bacteria. Results We report pan-genomic analysis of sixteen species from genus Chlamydia including identification and functional annotation of orthologous genes, and characterization of gene gains, losses, and rearrangements. We demonstrate the overall genome stability of these bacteria as indicated by a large fraction of common genes with conserved genomic locations. On the other hand, extreme evolvability is confined to several paralogous gene families such as polymorphic membrane proteins and phospholipase D, and likely is caused by the pressure from the host immune system. Conclusions This combination of a large, conserved core genome and a small, evolvable periphery likely reflect the balance between the selective pressure towards genome reduction and the need to adapt to escape from the host immunity.

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Phylogenomics reveals that Asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene

10.1101/2020.10.30.363036 ◽

2020 ◽

Author(s):

Francesco Comandatore ◽

Claudia Damiani ◽

Alessia Cappelli ◽

Paulo Ribolla ◽

Giuliano Gasperi ◽

...

Keyword(s):

Metabolic Pathways ◽

Genome Stability ◽

Pyrethroid Resistance ◽

Mosquito Species ◽

Genome Reduction ◽

Phylogenomic Analysis ◽

Symbiotic Association ◽

Symbiotic Relationship ◽

Common Pattern

AbstractThe mosquito microbiota is composed by several lineages of microorganisms whose ecological roles and evolutionary histories have yet to be investigated in depth. Among these microorganisms, Asaia bacteria play a prominent role, given its abundance in the gut, reproductive organs and salivary glands of different mosquito species, while its presence has also been reported in several other insects. Notably, Asaia has great potential as a tool for the control of mosquito-borne diseases. Here, we present a wide phylogenomic analysis of Asaia strains isolated from different species of mosquito vectors and from different populations of the Mediterranean fruit fly (medfly) Ceratitis capitata, an insect pest of worldwide economic importance. We show that phylogenetically distant lineages of Asaia experienced independent genome reductions, despite following a common pattern, characterized by the early loss of genes involved in genome stability. This result highlights the role of specific metabolic pathways in the symbiotic relationship between Asaia and the insect host. Finally, we discovered that all but one of the Asaia strains included in the study possess the pyrethroid hydrolase gene. Phylogenetic analysis revealed that this gene is ancestral in Asaia, strongly suggesting that it played a role in the establishment of the symbiotic association between these bacteria and the mosquito hosts. We propose that this gene from the symbiont contributed to initial pyrethroid resistance in insects harboring Asaia, also considering the widespread production of pyrethrins by several plants.ImportanceWe have studied genome reduction within several strains of the insect symbiont Asaia, isolated from different species/strains of mosquito and medfly. Phylogenetically distant strains of Asaia, despite following a common pattern involving the loss of genes related to genome stability, have undergone independent genome reductions, highlighting the peculiar role of specific metabolic pathways in the symbiotic relationship between Asaia and its host. We also show that the pyrethroid hydrolase gene is present in all the Asaia strains isolated except for the South American malaria vector An. darlingi, for which resistance to pyrethroids has never been reported, suggesting a possible involvement of Asaia in determining the resistance to insecticides.

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Phylogenomics Reveals that Asaia Symbionts from Insects Underwent Convergent Genome Reduction, Preserving an Insecticide-Degrading Gene

mBio ◽

10.1128/mbio.00106-21 ◽

2021 ◽

Vol 12 (2) ◽

Author(s):

Francesco Comandatore ◽

Claudia Damiani ◽

Alessia Cappelli ◽

Paulo Eduardo Martins Ribolla ◽

Giuliano Gasperi ◽

...

Keyword(s):

Metabolic Pathways ◽

Genome Stability ◽

Pyrethroid Resistance ◽

Mosquito Species ◽

Genome Reduction ◽

Phylogenomic Analysis ◽

Symbiotic Association ◽

Symbiotic Relationship ◽

Common Pattern

ABSTRACT The mosquito microbiota is composed of several lineages of microorganisms whose ecological roles and evolutionary histories have yet to be investigated in depth. Among these microorganisms, Asaia bacteria play a prominent role, given their abundance in the gut, reproductive organs, and salivary glands of different mosquito species, while their presence has also been reported in several other insects. Notably, Asaia has great potential as a tool for the control of mosquito-borne diseases. Here, we present a wide phylogenomic analysis of Asaia strains isolated from different species of mosquito vectors and from different populations of the Mediterranean fruit fly (medfly), Ceratitis capitata, an insect pest of worldwide economic importance. We show that phylogenetically distant lineages of Asaia experienced independent genome reductions, despite following a common pattern, characterized by the early loss of genes involved in genome stability. This result highlights the role of specific metabolic pathways in the symbiotic relationship between Asaia and the insect host. Finally, we discovered that all but one of the Asaia strains included in the study possess the pyrethroid hydrolase gene. Phylogenetic analysis revealed that this gene is ancestral in Asaia, strongly suggesting that it played a role in the establishment of the symbiotic association between these bacteria and the mosquito hosts. We propose that this gene from the symbiont contributed to initial pyrethroid resistance in insects harboring Asaia, also considering the widespread production of pyrethrins by several plants. IMPORTANCE We have studied genome reduction within several strains of the insect symbiont Asaia isolated from different species/strains of mosquito and medfly. Phylogenetically distant strains of Asaia, despite following a common pattern involving the loss of genes related to genome stability, have undergone independent genome reductions, highlighting the peculiar role of specific metabolic pathways in the symbiotic relationship between Asaia and its host. We also show that the pyrethroid hydrolase gene is present in all the Asaia strains isolated except for the South American malaria vector Anopheles darlingi, for which resistance to pyrethroids has never been reported, suggesting a possible involvement of Asaia in determining resistance to insecticides.

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