Genome reduction and relaxed selection is associated with the transition to symbiosis in the basidiomycete genus Podaxis

ABSTRACTVarious intracellular bacterial symbionts that provide their host with essential nutrients have much-reduced genomes, attributed largely to genomic decay and relaxed selection. To obtain quantitative estimates of the metabolic function of these bacteria, we reconstructed genome- and transcriptome-informed metabolic models of three xylem-feeding insects that bear two bacterial symbionts with complementary metabolic functions: a primary symbiont,Sulcia, that has codiversified with the insects, and a coprimary symbiont of distinct taxonomic origin and with different degrees of genome reduction in each insect species (Hodgkiniain a cicada,Baumanniain a sharpshooter, andSodalisin a spittlebug). Our simulations reveal extensive bidirectional flux of multiple metabolites between each symbiont and the host, but near-complete metabolic segregation (i.e., near absence of metabolic cross-feeding) between the two symbionts, a likely mode of host control over symbiont metabolism. Genome reduction of the symbionts is associated with an increased number of host metabolic inputs to the symbiont and also reduced metabolic cost to the host. In particular,SulciaandHodgkiniawith genomes of ≤0.3 Mb are calculated to recycle ∼30 to 80% of host-derived nitrogen to essential amino acids returned to the host, whileBaumanniaandSodaliswith genomes of ≥0.6 Mb recycle 10 to 15% of host nitrogen. We hypothesize that genome reduction of symbionts may be driven by selection for increased host control and reduced host costs, as well as by the stochastic process of genomic decay and relaxed selection.IMPORTANCECurrent understanding of many animal-microbial symbioses involving unculturable bacterial symbionts with much-reduced genomes derives almost entirely from nonquantitative inferences from genome data. To overcome this limitation, we reconstructed multipartner metabolic models that quantify both the metabolic fluxes within and between three xylem-feeding insects and their bacterial symbionts. This revealed near-complete metabolic segregation between cooccurring bacterial symbionts, despite extensive metabolite exchange between each symbiont and the host, suggestive of strict host controls over the metabolism of its symbionts. We extended the model analysis to investigate metabolic costs. The positive relationship between symbiont genome size and the metabolic cost incurred by the host points to fitness benefits to the host of bearing symbionts with small genomes. The multicompartment metabolic models developed here can be applied to other symbioses that are not readily tractable to experimental approaches.

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Independent pseudogenizations and losses of sox15 during amniote diversification following asymmetric ohnolog evolution

BMC Ecology and Evolution ◽

10.1186/s12862-021-01864-z ◽

2021 ◽

Vol 21 (1) ◽

Author(s):

Yusaku Ogita ◽

Kei Tamura ◽

Shuuji Mawaribuchi ◽

Nobuhiko Takamatsu ◽

Michihiko Ito

Keyword(s):

Sequence Similarity ◽

The Other ◽

Vertebrate Evolution ◽

Skeletal Muscle Regeneration ◽

Cns Development ◽

Placental Development ◽

Relaxed Selection ◽

Significant Sequence Similarity ◽

Anuran Amphibians ◽

Divergent Gene

Abstract Background Four ohnologous genes (sox1, sox2, sox3, and sox15) were generated by two rounds of whole-genome duplication in a vertebrate ancestor. In eutherian mammals, Sox1, Sox2, and Sox3 participate in central nervous system (CNS) development. Sox15 has a function in skeletal muscle regeneration and has little functional overlap with the other three ohnologs. In contrast, the frog Xenopus laevis and zebrafish orthologs of sox15 as well as sox1-3 function in CNS development. We previously reported that Sox15 is involved in mouse placental development as neofunctionalization, but is pseudogenized in the marsupial opossum. These findings suggest that sox15 might have evolved with divergent gene fates during vertebrate evolution. However, knowledge concerning sox15 in other vertebrate lineages than therian mammals, anuran amphibians, and teleost fish is scarce. Our purpose in this study was to clarify the fate and molecular evolution of sox15 during vertebrate evolution. Results We searched for sox15 orthologs in all vertebrate classes from agnathans to mammals by significant sequence similarity and synteny analyses using vertebrate genome databases. Interestingly, sox15 was independently pseudogenized at least twice during diversification of the marsupial mammals. Moreover, we observed independent gene loss of sox15 at least twice during reptile evolution in squamates and crocodile-bird diversification. Codon-based phylogenetic tree and selective analyses revealed an increased dN/dS ratio for sox15 compared to the other three ohnologs during jawed vertebrate evolution. Conclusions The findings revealed an asymmetric evolution of sox15 among the four ohnologs during vertebrate evolution, which was supported by the increased dN/dS values in cartilaginous fishes, anuran amphibians, and amniotes. The increased dN/dS value of sox15 may have been caused mainly by relaxed selection. Notably, independent pseudogenizations and losses of sox15 were observed during marsupial and reptile evolution, respectively. Both might have been caused by strong relaxed selection. The drastic gene fates of sox15, including neofunctionalization and pseudogenizations/losses during amniote diversification, might be caused by a release from evolutionary constraints.

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Sequence of a Coxiella endosymbiont of the tick Amblyomma nuttalli suggests a pattern of convergent genome reduction in the Coxiella genus

Genome Biology and Evolution ◽

10.1093/gbe/evaa253 ◽

2020 ◽

Author(s):

Tiago Nardi ◽

Emanuela Olivieri ◽

Edward Kariuki ◽

Davide Sassera ◽

Michele Castelli

Keyword(s):

Coxiella Burnetii ◽

Phylogenetic Analyses ◽

Genome Reduction ◽

Metabolic Profiles ◽

The Novel ◽

Bacterial Symbionts ◽

Human Pathogen ◽

Host Genus ◽

Supportive Role ◽

Genus One

Abstract Ticks require bacterial symbionts for the provision of necessary compounds that are absent in their hematophagous diet. Such symbionts are frequently vertically transmitted and, most commonly, belong to the Coxiella genus, which also includes the human pathogen Coxiella burnetii. This genus can be divided in four main clades, presenting partial but incomplete co-cladogenesis with the tick hosts. Here we report the genome sequence of a novel Coxiella, endosymbiont of the African tick Amblyomma nuttalli, and the ensuing comparative analyses. Its size (~1 Mb) is intermediate between symbionts of Rhipicephalus species and other Amblyomma species. Phylogenetic analyses show that the novel sequence is the first genome of the B clade, the only one for which no genomes were previously available. Accordingly, it allows to draw an enhanced scenario of the evolution of the genus, one of parallel genome reduction of different endosymbiont lineages, which are now at different stages of reduction from a more versatile ancestor. Gene content comparison allows to infer that the ancestor could be reminiscent of Coxiella burnetii. Interestingly, the convergent loss of mismatch repair could have been a major driver of such reductive evolution. Predicted metabolic profiles are rather homogenous among Coxiella endosymbionts, in particular vitamin biosynthesis, consistently with a host-supportive role. Concurrently, similarities among Coxiella endosymbionts according to host genus and despite phylogenetic unrelatedness hint at possible host-dependent effects.

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Publisher Correction: Relaxed selection underlies genome erosion in socially parasitic ant species

Nature Communications ◽

10.1038/s41467-021-23950-y ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Lukas Schrader ◽

Hailin Pan ◽

Martin Bollazzi ◽

Morten Schiøtt ◽

Fredrick J. Larabee ◽

...

Keyword(s):

Relaxed Selection

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Mechanisms driving genome reduction of a novel Roseobacter lineage

The ISME Journal ◽

10.1038/s41396-021-01036-3 ◽

2021 ◽

Author(s):

Xiaoyuan Feng ◽

Xiao Chu ◽

Yang Qian ◽

Michael W. Henson ◽

V. Celeste Lanclos ◽

...

Keyword(s):

Genome Reduction

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Genome Reduction and Secondary Metabolism of the Marine Sponge-Associated Cyanobacterium Leptothoe

Marine Drugs ◽

10.3390/md19060298 ◽

2021 ◽

Vol 19 (6) ◽

pp. 298

Author(s):

Despoina Konstantinou ◽

Rafael V. Popin ◽

David P. Fewer ◽

Kaarina Sivonen ◽

Spyros Gkelis

Keyword(s):

Natural Products ◽

Microbial Communities ◽

Genomic Analysis ◽

Gene Clusters ◽

Marine Sponges ◽

Genome Reduction ◽

Extracellular Polysaccharides ◽

Comparative Genomic ◽

Symbiotic Relationships ◽

Genes Encoding

Sponges form symbiotic relationships with diverse and abundant microbial communities. Cyanobacteria are among the most important members of the microbial communities that are associated with sponges. Here, we performed a genus-wide comparative genomic analysis of the newly described marine benthic cyanobacterial genus Leptothoe (Synechococcales). We obtained draft genomes from Le. kymatousa TAU-MAC 1615 and Le. spongobia TAU-MAC 1115, isolated from marine sponges. We identified five additional Leptothoe genomes, host-associated or free-living, using a phylogenomic approach, and the comparison of all genomes showed that the sponge-associated strains display features of a symbiotic lifestyle. Le. kymatousa and Le. spongobia have undergone genome reduction; they harbored considerably fewer genes encoding for (i) cofactors, vitamins, prosthetic groups, pigments, proteins, and amino acid biosynthesis; (ii) DNA repair; (iii) antioxidant enzymes; and (iv) biosynthesis of capsular and extracellular polysaccharides. They have also lost several genes related to chemotaxis and motility. Eukaryotic-like proteins, such as ankyrin repeats, playing important roles in sponge-symbiont interactions, were identified in sponge-associated Leptothoe genomes. The sponge-associated Leptothoe stains harbored biosynthetic gene clusters encoding novel natural products despite genome reduction. Comparisons of the biosynthetic capacities of Leptothoe with chemically rich cyanobacteria revealed that Leptothoe is another promising marine cyanobacterium for the biosynthesis of novel natural products.

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