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

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. <i>Trichosphaerium</i>, a polymorphic, multinucleate, marine amoeba with a comp...

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Main Authors: Yonas I. Tekle, Hanh Tran, Fang Wang, Mandakini Singla, Isimeme Udu
Format: Article
Language:English
Published: MDPI AG 2023-05-01
Series:Microbiology Research
Subjects:
Online Access:https://www.mdpi.com/2036-7481/14/2/47
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author Yonas I. Tekle
Hanh Tran
Fang Wang
Mandakini Singla
Isimeme Udu
author_facet Yonas I. Tekle
Hanh Tran
Fang Wang
Mandakini Singla
Isimeme Udu
author_sort Yonas I. Tekle
collection DOAJ
description 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. <i>Trichosphaerium</i>, 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 <i>Trichosphaerium</i> 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 <i>Trichosphaerium</i> 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 <i>Trichosphaerium</i>, our genomic data showed that populations maintain a species-level intragenomic variation. A draft genome of <i>Trichosphaerium</i> indicates elevated lateral gene transfer (LGT) from bacteria and giant viruses. Gene trafficking in <i>Trichosphaerium</i> is the highest within Amoebozoa and among the highest in microbial eukaryotes.
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spelling doaj.art-1ef2d39a9bd147d9937441b2441d74022023-11-18T11:38:11ZengMDPI AGMicrobiology Research2036-74812023-05-0114265667210.3390/microbiolres14020047Omics of an Enigmatic Marine Amoeba Uncovers Unprecedented Gene Trafficking from Giant Viruses and Provides Insights into Its Complex Life CycleYonas I. Tekle0Hanh Tran1Fang Wang2Mandakini Singla3Isimeme Udu4Department of Biology, Spelman College, 350 Spelman Lane Southwest, Atlanta, GA 30314, USADepartment of Biology, Spelman College, 350 Spelman Lane Southwest, Atlanta, GA 30314, USADepartment of Biology, Spelman College, 350 Spelman Lane Southwest, Atlanta, GA 30314, USADepartment of Biology, Spelman College, 350 Spelman Lane Southwest, Atlanta, GA 30314, USADepartment of Biology, Spelman College, 350 Spelman Lane Southwest, Atlanta, GA 30314, USAAmoebozoa 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. <i>Trichosphaerium</i>, 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 <i>Trichosphaerium</i> 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 <i>Trichosphaerium</i> 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 <i>Trichosphaerium</i>, our genomic data showed that populations maintain a species-level intragenomic variation. A draft genome of <i>Trichosphaerium</i> indicates elevated lateral gene transfer (LGT) from bacteria and giant viruses. Gene trafficking in <i>Trichosphaerium</i> is the highest within Amoebozoa and among the highest in microbial eukaryotes.https://www.mdpi.com/2036-7481/14/2/47genometranscriptomeamoebozoasexual reproductionmeiosishorizontal gene transfer
spellingShingle Yonas I. Tekle
Hanh Tran
Fang Wang
Mandakini Singla
Isimeme Udu
Omics of an Enigmatic Marine Amoeba Uncovers Unprecedented Gene Trafficking from Giant Viruses and Provides Insights into Its Complex Life Cycle
Microbiology Research
genome
transcriptome
amoebozoa
sexual reproduction
meiosis
horizontal gene transfer
title Omics of an Enigmatic Marine Amoeba Uncovers Unprecedented Gene Trafficking from Giant Viruses and Provides Insights into Its Complex Life Cycle
title_full Omics of an Enigmatic Marine Amoeba Uncovers Unprecedented Gene Trafficking from Giant Viruses and Provides Insights into Its Complex Life Cycle
title_fullStr Omics of an Enigmatic Marine Amoeba Uncovers Unprecedented Gene Trafficking from Giant Viruses and Provides Insights into Its Complex Life Cycle
title_full_unstemmed Omics of an Enigmatic Marine Amoeba Uncovers Unprecedented Gene Trafficking from Giant Viruses and Provides Insights into Its Complex Life Cycle
title_short Omics of an Enigmatic Marine Amoeba Uncovers Unprecedented Gene Trafficking from Giant Viruses and Provides Insights into Its Complex Life Cycle
title_sort omics of an enigmatic marine amoeba uncovers unprecedented gene trafficking from giant viruses and provides insights into its complex life cycle
topic genome
transcriptome
amoebozoa
sexual reproduction
meiosis
horizontal gene transfer
url https://www.mdpi.com/2036-7481/14/2/47
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