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1. Opinion: Genetic Conflict With Mobile Elements Drives Eukaryotic Genome Evolution, and Perhaps Also Eukaryogenesis

   https://doi.org/10.1093/jhered/esaa060  

   Collens, Adena B ; Katz, Laura A ( January 2021 , Journal of Heredity)

   Orive, Maria (Ed.)

   Abstract Through analyses of diverse microeukaryotes, we have previously argued that eukaryotic genomes are dynamic systems that rely on epigenetic mechanisms to distinguish germline (i.e., DNA to be inherited) from soma (i.e., DNA that undergoes polyploidization, genome rearrangement, etc.), even in the context of a single nucleus. Here, we extend these arguments by including two well-documented observations: (1) eukaryotic genomes interact frequently with mobile genetic elements (MGEs) like viruses and transposable elements (TEs), creating genetic conflict, and (2) epigenetic mechanisms regulate MGEs. Synthesis of these ideas leads to the hypothesis that genetic conflict with MGEs contributed to the evolution of a dynamic eukaryotic genome in the last eukaryotic common ancestor (LECA), and may have contributed to eukaryogenesis (i.e., may have been a driver in the evolution of FECA, the first eukaryotic common ancestor). Sex (i.e., meiosis) may have evolved within the context of the development of germline–soma distinctions in LECA, as this process resets the germline genome by regulating/eliminating somatic (i.e., polyploid, rearranged) genetic material. Our synthesis of these ideas expands on hypotheses of the origin of eukaryotes by integrating the roles of MGEs and epigenetics. 

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2. Genome architecture used to supplement species delineation in two cryptic marine ciliates

   https://doi.org/10.1111/1755-0998.13664  

   Smith, Susan A. ; Santoferrara, Luciana F. ; Katz, Laura A. ; McManus, George B. ( June 2022 , Molecular Ecology Resources)

   The purpose of this study is to determine which taxonomic methods can elucidate clear and quantifiable differences between two cryptic ciliate species, and to test the utility of genome architecture as a new diagnostic character in the discrimination of otherwise indistinguishable taxa. Two cryptic tintinnid ciliates,Schmidingerella arcuataandSchmidingerella meunieri, are compared via traditional taxonomic characters including lorica morphometrics, ribosomal RNA (rRNA) gene barcodes and ecophysiological traits. In addition, single‐cell ‘omics analyses (single‐cell transcriptomics and genomics) are used to elucidate and compare patterns of micronuclear genome architecture between the congeners. The results include a highly similar lorica that is larger inS. meunieri, a 0%–0.5% difference in rRNA gene barcodes, two different and nine indistinguishable growth responses among 11 prey treatments, and distinct patterns of micronuclear genomic architecture for genes detected in both ciliates. Together, these results indicate that while minor differences exist betweenS. arcuataandS. meunieriin common indices of taxonomic identification (i.e., lorica morphology, DNA barcode sequences and ecophysiology), differences exist in their genomic architecture, which suggests potential genetic incompatibility. Different patterns of micronuclear architecture in genes shared by both isolates also enable the design of species‐specific primers, which are used in this study as unique “architectural barcodes” to demonstrate the co‐occurrence of both ciliates in samples collected from a NW Atlantic estuary. These results support the utility of genomic architecture as a tool in species delineation, especially in ciliates that are cryptic or otherwise difficult to differentiate using traditional methods of identification.

    

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3. Sex, amitosis, and evolvability in the ciliate Tetrahymena thermophila

   https://doi.org/10.1093/evolut/qpac031  

   Tarkington, Jason ; Zhang, Hao ; Azevedo, Ricardo B. R. ; Zufall, Rebecca A. ( December 2022 , Evolution)

   Understanding the mechanisms that generate genetic variation, and thus contribute to the process of adaptation, is a major goal of evolutionary biology. Mutation and genetic exchange have been well studied as mechanisms to generate genetic variation. However, there are additional factors, such as genome architecture, that may also impact the amount of genetic variation in some populations, and the extent to which these variation generating mechanisms are themselves shaped by natural selection is still an open question. To test the effect of genome architecture on the generation of genetic variation, and hence evolvability, we studied Tetrahymena thermophila, a ciliate with an unusual genome structure and mechanism of nuclear division, called amitosis, whereby homologous chromosomes are randomly distributed to daughter cells. Amitosis leads to genetic variation among the asexual descendants of a newly produced sexual progeny because different progeny cells will contain different combinations of parental alleles. We hypothesize that amitosis thus increases the evolvability of newly produced sexual progeny relative to their unmated parents and species that undergo mitosis. To test this hypothesis, we used experimental evolution and simulations to compare the rate of adaptation in T. thermophila populations founded by a single sexual progeny to parental populations that had not had sex in many generations. The populations founded by a sexual progeny adapted more quickly than parental populations in both laboratory populations and simulated populations. This suggests that the additional genetic variation generated by amitosis of a heterozygote can increase the rate of adaptation following sex and may help explain the evolutionary success of the unusual genetic architecture of Tetrahymena and ciliates more generally.

    

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4. Mobile elements create strain‐level variation in the services conferred by an aphid symbiont

   https://doi.org/10.1111/1462-2920.16520  

   Patel, Vilas ; Lynn‐Bell, Nicole ; Chevignon, Germain ; Kucuk, Roy A. ; Higashi, Clesson H. V. ; Carpenter, Melissa ; Russell, Jacob A. ; Oliver, Kerry M. ( October 2023 , Environmental Microbiology)

   Heritable, facultative symbionts are common in arthropods, often functioning in host defence. Despite moderately reduced genomes, facultative symbionts retain evolutionary potential through mobile genetic elements (MGEs). MGEs form the primary basis of strain‐level variation in genome content and architecture, and often correlate with variability in symbiont‐mediated phenotypes. In pea aphids (Acyrthosiphon pisum), strain‐level variation in the type of toxin‐encoding bacteriophages (APSEs) carried by the bacteriumHamiltonella defensacorrelates with strength of defence against parasitoids. However, co‐inheritance creates difficulties for partitioning their relative contributions to aphid defence. Here we identified isolates ofH. defensathat were nearly identical except for APSE type. When holdingH. defensagenotype constant, protection levels corresponded to APSE virulence module type. Results further indicated that APSEs move repeatedly within someH. defensaclades providing a mechanism for rapid evolution in anti‐parasitoid defences. Strain variation inH. defensaalso correlates with the presence of a second symbiontFukatsuia symbiotica. Predictions that nutritional interactions structured this coinfection were not supported by comparative genomics, but bacteriocin‐containing plasmids unique to co‐infecting strains may contribute to their common pairing. In conclusion, strain diversity, and joint capacities for horizontal transfer of MGEs and symbionts, are emergent players in the rapid evolution of arthropods.

    

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5. Transcribed germline-limited coding sequences in Oxytricha trifallax

   https://doi.org/10.1093/g3journal/jkab092  

   Miller, Richard V ; Neme, Rafik ; Clay, Derek M ; Pathmanathan, Jananan S ; Lu, Michael W ; Yerlici, V Talya ; Khurana, Jaspreet S ; Landweber, Laura F ( June 2021 , G3 Genes|Genomes|Genetics)

   Hughes, T (Ed.)

   Abstract The germline-soma divide is a fundamental distinction in developmental biology, and different genes are expressed in germline and somatic cells throughout metazoan life cycles. Ciliates, a group of microbial eukaryotes, exhibit germline-somatic nuclear dimorphism within a single cell with two different genomes. The ciliate Oxytricha trifallax undergoes massive RNA-guided DNA elimination and genome rearrangement to produce a new somatic macronucleus (MAC) from a copy of the germline micronucleus (MIC). This process eliminates noncoding DNA sequences that interrupt genes and also deletes hundreds of germline-limited open reading frames (ORFs) that are transcribed during genome rearrangement. Here, we update the set of transcribed germline-limited ORFs (TGLOs) in O. trifallax. We show that TGLOs tend to be expressed during nuclear development and then are absent from the somatic MAC. We also demonstrate that exposure to synthetic RNA can reprogram TGLO retention in the somatic MAC and that TGLO retention leads to transcription outside the normal developmental program. These data suggest that TGLOs represent a group of developmentally regulated protein-coding sequences whose gene expression is terminated by DNA elimination. 

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