The draft genome of Cochliopodium minus reveals a complete meiosis toolkit and provides insight into the evolution of sexual mechanisms in Amoebozoa

Tekle, Yonas I.; Wang, Fang; Tran, Hanh; Hayes, T. Danielle; Ryan, Joseph F.

doi:10.1038/s41598-022-14131-y

Cited by 2 publications

(19 citation statements)

References 55 publications

(113 reference statements)

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“…As previously observed (Fritz-Laylin et al, 2010;Herman et al, 2021), we also noticed that some of these genes (e.g., RAD51, HAP2, MSH6, SPO11) have several paralogs and certain meiosisspecific genes are differentially present in Naegleria species (N. fowleri 986 presenting the highest number of gene paralogs namely for HAP2, MSH5, MLH1, MSH6 and MLH4, Supplementary Table S6). This variation in sexual mechanism has been previously reported for amoebozoans (Tekle et al, 2017(Tekle et al, , 2022 and Symbiodiniaceae dinoflagellates (Shah et al, 2020).…”

Section: Life Cycle and Reproductionsupporting

confidence: 82%

Naegleria genus pangenome reveals new structural and functional insights into the versatility of these free-living amoebae

et al. 2023

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IntroductionFree-living amoebae of the Naegleria genus belong to the major protist clade Heterolobosea and are ubiquitously distributed in soil and freshwater habitats. Of the 47 Naegleria species described, N. fowleri is the only one being pathogenic to humans, causing a rare but fulminant primary amoebic meningoencephalitis. Some Naegleria genome sequences are publicly available, but the genetic basis for Naegleria diversity and ability to thrive in diverse environments (including human brain) remains unclear.MethodsHerein, we constructed a high-quality Naegleria genus pangenome to obtain a comprehensive catalog of genes encoded by these amoebae. For this, we first sequenced, assembled, and annotated six new Naegleria genomes.Results and DiscussionGenome architecture analyses revealed that Naegleria may use genome plasticity features such as ploidy/aneuploidy to modulate their behavior in different environments. When comparing 14 near-to-complete genome sequences, our results estimated the theoretical Naegleria pangenome as a closed genome, with 13,943 genes, including 3,563 core and 10,380 accessory genes. The functional annotations revealed that a large fraction of Naegleria genes show significant sequence similarity with those already described in other kingdoms, namely Animalia and Plantae. Comparative analyses highlighted a remarkable genomic heterogeneity, even for closely related strains and demonstrate that Naegleria harbors extensive genome variability, reflected in different metabolic repertoires. If Naegleria core genome was enriched in conserved genes essential for metabolic, regulatory and survival processes, the accessory genome revealed the presence of genes involved in stress response, macromolecule modifications, cell signaling and immune response. Commonly reported N. fowleri virulence-associated genes were present in both core and accessory genomes, suggesting that N. fowleri’s ability to infect human brain could be related to its unique species-specific genes (mostly of unknown function) and/or to differential gene expression. The construction of Naegleria first pangenome allowed us to move away from a single reference genome (that does not necessarily represent each species as a whole) and to identify essential and dispensable genes in Naegleria evolution, diversity and biology, paving the way for further genomic and post-genomic studies.

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Section: Life Cycle and Reproductionsupporting

confidence: 82%

Naegleria genus pangenome reveals new structural and functional insights into the versatility of these free-living amoebae

et al. 2023

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“…The taxonomic distribution of predicted gene models in the Trichosphaerium sp. draft genome followed a general pattern with other amoebae genomes [ 32 – 34 ] but with higher percentages of laterally transferred genes. About 74% of the predicted gene models matched to eukaryotic (47.6%) and ORFan (26.5%) genes ( Figure 3 ).…”

Section: Resultsmentioning

confidence: 77%

“…We followed the methodology for gene annotation described in Tekle et al [ 32 ] using transcriptome data collected from various samples of Trichosphaerium sp. and protein sequences from a published genome of a related amoeba, Acanthamoeba castellanii [ 33 ].…”

Section: Methodsmentioning

confidence: 99%

“…We performed BLASTP to search these genes against archaea, bacteria, and virus genomes that were commonly seen in previous BLAST results. We then performed an Alien Index (AI) analysis on the BLASTP results similar to the methods described in Tekle et al [ 32 ] to calculate the AI scores. Genes with AI ≥ 45 were considered as putative LTGs.…”

Section: Methodsmentioning

confidence: 99%

“…To identify gene models implicated in sexual reproduction in the draft genome of Trichosphaerium sp., we performed a BLASTP (e-value 1 × 10 −15 ) search of over 90 genes including 12 meiosis-specific and sex-related genes, as described in Wood et al [ 31 ]. The selected genes were further analyzed using phylogenetic analysis in IQ-Tree, as described in Tekle et al [ 32 ], to further assess their homology in the phylogenetic framework.…”

Section: Methodsmentioning

confidence: 99%

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Omics of an Enigmatic Marine Amoeba Uncovers Unprecedented Gene Trafficking from Giant Viruses and Provides Insights into Its Complex Life Cycle

Tekle

Tran

Wang

et al. 2023

Microbiology Research

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Amoebozoa include lineages of diverse ecology, behavior, and morphology. They are assumed to encompass members with the largest genome sizes of all living things, yet genomic studies in the group are limited. Trichosphaerium, a polymorphic, multinucleate, marine amoeba with a complicated life cycle, has puzzled experts for over a century. In an effort to explore the genomic diversity and investigate extraordinary behavior observed among the Amoebozoa, we used integrated omics approaches to study this enigmatic marine amoeba. Omics data, including single-cell transcriptomics and cytological data, demonstrate that Trichosphaerium sp. possesses the complete meiosis toolkit genes. These genes are expressed in life stages of the amoeba including medium and large cells. The life cycle of Trichosphaerium sp. involves asexual processes via binary fission and multiple fragmentation of giant cells, as well as sexual-like processes involving genes implicated in sexual reproduction and polyploidization. These findings are in stark contrast to a life cycle previously reported for this amoeba. Despite the extreme morphological plasticity observed in Trichosphaerium, our genomic data showed that populations maintain a species-level intragenomic variation. A draft genome of Trichosphaerium indicates elevated lateral gene transfer (LGT) from bacteria and giant viruses. Gene trafficking in Trichosphaerium is the highest within Amoebozoa and among the highest in microbial eukaryotes.

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The draft genome of Cochliopodium minus reveals a complete meiosis toolkit and provides insight into the evolution of sexual mechanisms in Amoebozoa

Cited by 2 publications

References 55 publications

Naegleria genus pangenome reveals new structural and functional insights into the versatility of these free-living amoebae

Naegleria genus pangenome reveals new structural and functional insights into the versatility of these free-living amoebae

Omics of an Enigmatic Marine Amoeba Uncovers Unprecedented Gene Trafficking from Giant Viruses and Provides Insights into Its Complex Life Cycle

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