Time-resolved small RNA transcriptomics of the ichthyosporean <i>Sphaeroforma arctica</i>

Andrej Ondracka; Omaya Dudin; Jon Bråte

doi:10.12688/f1000research.133935.1

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Data Note

Time-resolved small RNA transcriptomics of the ichthyosporean Sphaeroforma arctica

[version 1; peer review: 2 approved]

Andrej Ondracka¹, Omaya Dudin², Jon Bråte ^3,4

PUBLISHED 24 May 2023

Author details Author details

¹ Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain
² Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology (EPFL), Lausanne, 1015, Switzerland
³ Department of Biosciences, University of Oslo, Oslo, 0316, Norway
⁴ Department of Virology, Norwegian Institute of Public Health, Oslo, 0456, Norway

Andrej Ondracka
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Omaya Dudin
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Jon Bråte
Roles: Formal Analysis, Funding Acquisition, Project Administration, Software, Supervision, Validation, Writing – Review & Editing

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Abstract

Ichthyosporea, a clade of holozoans, represent a clade closely related to animals, and thus hold a key phylogenetic position for understanding the origin of animals. We have previously discovered that an ichthyosporean, Sphaeroforma arctica, contains microRNAs (miRNAs) as well as the miRNA processing machinery. This was the first discovery of miRNAs among the closest single-celled relatives of animals and raised intriguing questions about the roles of regulatory small RNAs in cell development and differentiation in unicellular eukaryotes. Like many ichthyosporeans, S. arctica also undergoes a transient multicellular developmental life cycle. As miRNAs are, among other roles, key regulators of gene expression during development in animals, we wanted to investigate the dynamics of miRNAs during the developmental cycle in S. arctica. Here we have therefore collected a comprehensive time-resolved small RNA transcriptome linked to specific life stages with a substantially higher sequencing depth than before, which can enable further discovery of functionally relevant small RNAs. The data consists of Illumina-sequenced small RNA libraries from two independent biological replicates of the entire life cycle of S. arctica with high temporal resolution. The dataset is directly linked and comes from the same samples as a previously published mRNA-seq dataset, thus enabling direct cross-functional analyses.

Keywords

Ichthyosporea, Sphaeroforma arctica, small RNA, microRNA, miRNA, gene regulation, cell differentiation, origin of animals

Corresponding author: Jon Bråte

Competing interests: No competing interests were disclosed.

Grant information: AO was supported by H2020 Marie Skłodowska-Curie Actions (Individual fellowship MSCA-IF 747086). OD was funded by a Swiss National Science Foundation Early PostDoc Mobility fellowship (P2LAP3_171815), a Marie Sklodowska-Curie individual fellowship (MSCA-IF 746044), and an Ambizione fellowship from the Swiss National Science Foundation (PZ00P3_185859). JB was supported by the Research Council of Norway (Young Research Talents grant 240284).
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2023 Ondracka A et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: Ondracka A, Dudin O and Bråte J. Time-resolved small RNA transcriptomics of the ichthyosporean Sphaeroforma arctica [version 1; peer review: 2 approved]. F1000Research 2023, 12:542 (https://doi.org/10.12688/f1000research.133935.1) First published: 24 May 2023, 12:542 (https://doi.org/10.12688/f1000research.133935.1) Latest published: 24 May 2023, 12:542 (https://doi.org/10.12688/f1000research.133935.1)

Introduction

Ichthyosporeans hold a key position in the evolutionary tree for understanding the origin of animals and animal multicellularity. Ichthyosporea is a clade of holozoans, of which many characterized representatives undergo multinucleate (coenocytic) life cycles and exhibit a transient multicellular stage during cellularization of the coenocytes.¹^,² Among ichthyosporeans, the life cycle of Sphaeroforma arctica has been best characterized. Multiple nuclear division cycles in a single cell occur with highly regular timing, forming multinuclear coenocytes,³ which is followed by actomyosin-dependent cellularization.⁴ The whole life cycle has been characterized through mRNA transcriptomics, showing dynamic transcriptional regulation during the life cycle, including transcriptional regulation of the putative key regulators of cellularization.⁴

microRNAs (miRNAs) are short RNA molecules that, among many roles, regulate the activity of genes important for multicellular development in both animals and plants (e.g., Refs. 5, 6). Although miRNAs have been reported from other eukaryote groups spanning the tree of life, such as brown and green algae (e.g., Refs. 7, 8) Amoebozoa (e.g., Ref. 9) excavates (e.g., Ref. 10) and unicellular Holozoa,¹¹ their presence and function in many cases remain controversial.¹² Nevertheless, these discoveries raise the intriguing question of whether small regulatory RNAs also play a role during development in unicellular and facultatively multicellular organisms. To understand whether miRNAs play a role in its development, we collected a high-quality small RNA dataset in S. arctica at both high depth and high temporal resolution throughout its entire developmental cycle.

Methods

The purpose of this study was to generate a dataset in order to (1) investigate the temporal dynamics of miRNA expression in S. arctica and to provide potential functional insights into the miRNAs, (2) discover novel miRNA genes in S. arctica, and (3) discover other potentially functionally relevant small RNAs, such as piRNAs (e.g., Refs. 13, 14).

We have acquired high throughput sequencing datasets of the fraction of RNA molecules smaller than approximately 200 nucleotides (small RNAs). We have isolated and sequenced the small RNA content from synchronized cultures every six hours over a period of 72 hours, spanning the entire cell cycle. The sequencing was done in two biological replicates. The experiment was performed in parallel with the previously published mRNA transcriptome dataset⁴ and the small RNA libraries were prepared from the same total RNA samples; thus, the present dataset can be analyzed simultaneously with the mRNA data.

Experimental design and culturing conditions and RNA extraction

The cultures were prepared according to the protocol originally described in Ref. 4. In detail, S. arctica cells were cultured in Marine Broth media (Marine Broth, Difco BD, NJ, USA; 37.4 g/L) in sterile culture flasks at 12°C in dark conditions. The cultures were grown to a stationary phase, which has been shown to synchronize the coenocytic cycles (see Ref. 3). At the start of the experiment, the saturated cultures were diluted 1:300 into fresh marine broth media. Aliquots were collected every six hours for 72 hours, spanning an entire coenocytic life cycle. RNA was extracted using the miRNeasy Mini Kit (QIAGEN, Venlo, Netherlands) from approximately 50 mL of culture for each culture aliquot, and RNA integrity was evaluated using a Bioanalyzer 2100 (Agilent, CA, US).

Library preparation and sequencing details

The small RNA libraries were prepared using the NEBNext Small RNA Library Prep Set for Illumina (New England Biolabs, MA, US). A total of 50 bp single-end reads were obtained by sequencing the libraries on the Illumina HiSeq 2500 platform with the v4 chemistry and high output mode. Library preparation and sequencing was carried out by the CRG Genomics core unit, Barcelona, Spain. The data presented here is not processed in any way. The sequencing libraries contained on average 22.7 million reads (SD = 5.3 mill reads). Together, this data represents a more than 40-fold higher sequencing depth than the previous study,¹¹ where small RNA reads were obtained from only two samples.

Limitations

The small RNA extractions were sequenced as is, without any external, or spiked-in, controls.

Data availability

Underlying data

European Nucleotide Archive: Sphaeroforma arctica small RNAs. Accession number PRJEB55646; https://identifiers.org/ena.embl:PRJEB55646

Table 1 details the individual files under accession number PRJEB55646.

Table 1. Overview of the data files.

File name	File types (file extension)	Data repository and identifier (DOI or accession number)
BT12_24755_ATCACG.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128701)
BT18_24755_CGATGT.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128702)
BT24_24755_TTAGGC.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128703)
BT30_24755_TGACCA.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128704)
BT36_24755_ACAGTG.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128705)
BT42_24755_GCCAAT.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128706)
BT48_24755_CAGATC.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128707)
BT54_24755_ACTTGA.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128708)
BT60_24755_GATCAG.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128709)
BT66_24755_TAGCTT.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128710)
BT72_24755_GGCTAC.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128711)
CT0_27189_ACAGTG.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128712)
CT6_27189_TAGCTT.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128713)
CT12_27189_CGATGT.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128714)
CT18_27189_TGACCA.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128715)
CT24_27189_CAGATC.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128716)
CT30_27189_CCGTCC.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128717)
CT36_27189_ATGTCA.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128718)
CT42_27189_GTTTCG.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128719)
CT48_27189_CAACTA.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128720)
CT54_27189_CGGAAT.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128721)
CT60_27189_TCCCGA.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128722)
CT66_27189_GTAGAG.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128723)
CT72_27189_GTGAAA.fastq.gz	fastq (.fastq.gz)	European Nucleotide Archive (ERR10128724)

Data are available under the terms of the Creative Commons Zero “No rights reserved” data waiver (CC0 1.0 Public domain dedication).

Acknowledgements

We thank Arthur A. B. Haraldsen for discussions and valuable contributions to the project, and the CRG Genomics core unit for library preparation and sequencing.

References

1. Mendoza L, Taylor JW, Ajello L: The class mesomycetozoea: a heterogeneous group of microorganisms at the animal-fungal boundary. Annu. Rev. Microbiol. 2002; 56: 315–344. Publisher Full Text
2. Jøstensen J-P, Sperstad S, Johansen S, et al.: Molecular-phylogenetic, structural and biochemical features of a cold-adapted, marine ichthyosporean near the animal-fungal divergence, described from in vitro cultures. Eur. J. Protistol. 2002; 38: 93–104. Publisher Full Text
3. Ondracka A, Dudin O, Ruiz-Trillo I: Decoupling of Nuclear Division Cycles and Cell Size during the Coenocytic Growth of the Ichthyosporean Sphaeroforma arctica. Curr. Biol. 2018; 28: 1964–1969.e2. PubMed Abstract | Publisher Full Text | Free Full Text
4. Dudin O, Ondracka A, Grau-Bové X, et al.: A unicellular relative of animals generates a layer of polarized cells by actomyosin-dependent cellularization. elife. 2019; 8: e49801. PubMed Abstract | Publisher Full Text | Free Full Text
5. Bartel DP: Metazoan MicroRNAs. Cell. 2018; 173: 20–51. PubMed Abstract | Publisher Full Text | Free Full Text
6. Moran Y, Agron M, Praher D, et al.: The evolutionary origin of plant and animal microRNAs. Nat. Ecol. Evol. 2017; 1: 0027. PubMed Abstract | Publisher Full Text | Free Full Text
7. Cock JM, Liu F, Duan D, et al.: Rapid Evolution of microRNA Loci in the Brown Algae. Genome Biol. Evol. 2017; 9: 740–749. PubMed Abstract | Publisher Full Text | Free Full Text
8. Molnár A, Schwach F, Studholme D, et al.: miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature. 2007; 447: 1126–1129. PubMed Abstract | Publisher Full Text
9. Avesson L, Reimegård J, Wagner EG, et al.: MicroRNAs in Amoebozoa: deep sequencing of the small RNA population in the social amoeba Dictyostelium discoideum reveals developmentally regulated microRNAs. RNA. 2012; 18: 1771–1782. PubMed Abstract | Publisher Full Text | Free Full Text
10. Huang PJ, Lin WC, Chen SC, et al.: Identification of putative miRNAs from the deep-branching unicellular flagellates. Genomics. 2012; 99: 101–107. PubMed Abstract | Publisher Full Text
11. Bråte J, Neumann RS, Fromm B, et al.: Unicellular Origin of the Animal MicroRNA Machinery. Curr. Biol. 2018; 28: 3288–3295.e5. PubMed Abstract | Publisher Full Text | Free Full Text
12. Tarver JE, Donoghue PCJ, Peterson KJ: Do miRNAs have a deep evolutionary history? BioEssays. 2012; 34: 857–866. PubMed Abstract | Publisher Full Text
13. Ozata DM, Gainetdinov I, Zoch A, et al.: PIWI-interacting RNAs: small RNAs with big functions. Nat. Rev. Genet. 2019; 20: 89–108. PubMed Abstract | Publisher Full Text
14. Grimson A, Srivastava M, Fahey B, et al.: Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature. 2008; 455: 1193–1197. PubMed Abstract | Publisher Full Text | Free Full Text

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Version 1

VERSION 1 PUBLISHED 24 May 2023

Author details Author details

¹ Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain
² Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology (EPFL), Lausanne, 1015, Switzerland
³ Department of Biosciences, University of Oslo, Oslo, 0316, Norway
⁴ Department of Virology, Norwegian Institute of Public Health, Oslo, 0456, Norway

Andrej Ondracka
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Omaya Dudin
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Jon Bråte
Roles: Formal Analysis, Funding Acquisition, Project Administration, Software, Supervision, Validation, Writing – Review & Editing

Competing interests

No competing interests were disclosed.

Grant information

AO was supported by H2020 Marie Skłodowska-Curie Actions (Individual fellowship MSCA-IF 747086). OD was funded by a Swiss National Science Foundation Early PostDoc Mobility fellowship (P2LAP3_171815), a Marie Sklodowska-Curie individual fellowship (MSCA-IF 746044), and an Ambizione fellowship from the Swiss National Science Foundation (PZ00P3_185859). JB was supported by the Research Council of Norway (Young Research Talents grant 240284).
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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https://doi.org/10.12688/f1000research.133935.1

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© 2023 Ondracka A et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Ondracka A, Dudin O and Bråte J. Time-resolved small RNA transcriptomics of the ichthyosporean Sphaeroforma arctica [version 1; peer review: 2 approved]. F1000Research 2023, 12:542 (https://doi.org/10.12688/f1000research.133935.1)

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Reviewer Report 11 May 2024

Arkadiy Garber, Arizona State University, Tempe, Arizona, USA

Approved

https://doi.org/10.5256/f1000research.146953.r248045

In this data report, Ondracka and Dudin present a number of small RNA libraries corresponding to different life stages of ichthyosporean Sphaeroforma arctica. I believe that this data will be very useful to the research community. My only recommendation to the methods ... Continue reading

In this data report, Ondracka and Dudin present a number of small RNA libraries corresponding to different life stages of ichthyosporean Sphaeroforma arctica. I believe that this data will be very useful to the research community. My only recommendation to the methods would be to more explicitly state how S. arctica cells were processed for RNA extraction. For example, how were the cells lysed? Was there any centrifugation to pellet the cells or cell debris? Was there any rRNA depletion done during library prep?

Is the rationale for creating the dataset(s) clearly described?

Yes
Are the protocols appropriate and is the work technically sound?

Yes
Are sufficient details of methods and materials provided to allow replication by others?

Partly
Are the datasets clearly presented in a useable and accessible format?

Yes

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: My area of expertise is in microbiology, bioinformatics, and evolutionary biology. I also have a background in molecular biology (including DNA and RNA).

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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Reviewer Report 01 Apr 2024

Rafał Milanowski, University of Warsaw, Warsaw, Poland

Approved

https://doi.org/10.5256/f1000research.146953.r252697

Ichthyosporea is a group of Opisthokonta that plays a crucial role in discussions about the origins of animals and animal multicellularity. The Data Note article by Ondracka et al. describes the previously unpublished small RNA transcriptome associated with specific life ... Continue reading

Ichthyosporea is a group of Opisthokonta that plays a crucial role in discussions about the origins of animals and animal multicellularity. The Data Note article by Ondracka et al. describes the previously unpublished small RNA transcriptome associated with specific life stages of the ichthyosporean species Sphaeroforma arctica. This dataset holds the potential to facilitate further discovery of functionally relevant small RNAs in this species.

The methodological section of the manuscript provides detailed procedures for culturing, RNA extraction, library preparation, and sequencing, thereby enabling the replication of all experiments. Data files are well-organized, summarized in a table, and deposited in the RNA database under a unique accession number. The references are thoughtfully selected, offering opportunities for deeper exploration of the topic.

Is the rationale for creating the dataset(s) clearly described?

Yes
Are the protocols appropriate and is the work technically sound?

Yes
Are sufficient details of methods and materials provided to allow replication by others?

Yes
Are the datasets clearly presented in a useable and accessible format?

Yes

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Phylogeny, evolution and genomics of protists

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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Rafał Milanowski, University of Warsaw, Warsaw, Poland
Arkadiy Garber, Arizona State University, Tempe, USA

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Arkadiy Garber, Arizona State University, Tempe, Arizona, USA

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Approved

In this data report, Ondracka and Dudin present a number of small RNA libraries corresponding to different life stages of ichthyosporean Sphaeroforma arctica. I believe that this data will be very useful to the research community. My only recommendation to the methods would be to more explicitly state how S. arctica cells were processed for RNA extraction. For example, how were the cells lysed? Was there any centrifugation to pellet the cells or cell debris? Was there any rRNA depletion done during library prep?

Is the rationale for creating the dataset(s) clearly described?

Yes
Are the protocols appropriate and is the work technically sound?

Yes
Are sufficient details of methods and materials provided to allow replication by others?

Partly
Are the datasets clearly presented in a useable and accessible format?

Yes

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

My area of expertise is in microbiology, bioinformatics, and evolutionary biology. I also have a background in molecular biology (including DNA and RNA).

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

Respond to this report

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Reviewer Report

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01 Apr 2024 | for Version 1

Rafał Milanowski, University of Warsaw, Warsaw, Poland

11 Views Cite this report Responses(0)

Approved

Ichthyosporea is a group of Opisthokonta that plays a crucial role in discussions about the origins of animals and animal multicellularity. The Data Note article by Ondracka et al. describes the previously unpublished small RNA transcriptome associated with specific life stages of the ichthyosporean species Sphaeroforma arctica. This dataset holds the potential to facilitate further discovery of functionally relevant small RNAs in this species.

The methodological section of the manuscript provides detailed procedures for culturing, RNA extraction, library preparation, and sequencing, thereby enabling the replication of all experiments. Data files are well-organized, summarized in a table, and deposited in the RNA database under a unique accession number. The references are thoughtfully selected, offering opportunities for deeper exploration of the topic.

Is the rationale for creating the dataset(s) clearly described?

Yes
Are the protocols appropriate and is the work technically sound?

Yes
Are sufficient details of methods and materials provided to allow replication by others?

Yes
Are the datasets clearly presented in a useable and accessible format?

Yes

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Phylogeny, evolution and genomics of protists

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

Respond to this report

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[1] 1. Mendoza L, Taylor JW, Ajello L: The class mesomycetozoea: a heterogeneous group of microorganisms at the animal-fungal boundary. Annu. Rev. Microbiol. 2002; 56: 315–344. Publisher Full Text

[2] 2. Jøstensen J-P, Sperstad S, Johansen S, et al.: Molecular-phylogenetic, structural and biochemical features of a cold-adapted, marine ichthyosporean near the animal-fungal divergence, described from in vitro cultures. Eur. J. Protistol. 2002; 38: 93–104. Publisher Full Text

[3] 3. Ondracka A, Dudin O, Ruiz-Trillo I: Decoupling of Nuclear Division Cycles and Cell Size during the Coenocytic Growth of the Ichthyosporean Sphaeroforma arctica. Curr. Biol. 2018; 28: 1964–1969.e2. PubMed Abstract | Publisher Full Text | Free Full Text

[4] 4. Dudin O, Ondracka A, Grau-Bové X, et al.: A unicellular relative of animals generates a layer of polarized cells by actomyosin-dependent cellularization. elife. 2019; 8: e49801. PubMed Abstract | Publisher Full Text | Free Full Text

[5] 5. Bartel DP: Metazoan MicroRNAs. Cell. 2018; 173: 20–51. PubMed Abstract | Publisher Full Text | Free Full Text

[6] 6. Moran Y, Agron M, Praher D, et al.: The evolutionary origin of plant and animal microRNAs. Nat. Ecol. Evol. 2017; 1: 0027. PubMed Abstract | Publisher Full Text | Free Full Text

[7] 7. Cock JM, Liu F, Duan D, et al.: Rapid Evolution of microRNA Loci in the Brown Algae. Genome Biol. Evol. 2017; 9: 740–749. PubMed Abstract | Publisher Full Text | Free Full Text

[8] 8. Molnár A, Schwach F, Studholme D, et al.: miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature. 2007; 447: 1126–1129. PubMed Abstract | Publisher Full Text

[9] 9. Avesson L, Reimegård J, Wagner EG, et al.: MicroRNAs in Amoebozoa: deep sequencing of the small RNA population in the social amoeba Dictyostelium discoideum reveals developmentally regulated microRNAs. RNA. 2012; 18: 1771–1782. PubMed Abstract | Publisher Full Text | Free Full Text

[10] 10. Huang PJ, Lin WC, Chen SC, et al.: Identification of putative miRNAs from the deep-branching unicellular flagellates. Genomics. 2012; 99: 101–107. PubMed Abstract | Publisher Full Text

[11] 11. Bråte J, Neumann RS, Fromm B, et al.: Unicellular Origin of the Animal MicroRNA Machinery. Curr. Biol. 2018; 28: 3288–3295.e5. PubMed Abstract | Publisher Full Text | Free Full Text

[12] 12. Tarver JE, Donoghue PCJ, Peterson KJ: Do miRNAs have a deep evolutionary history? BioEssays. 2012; 34: 857–866. PubMed Abstract | Publisher Full Text

[13] 13. Ozata DM, Gainetdinov I, Zoch A, et al.: PIWI-interacting RNAs: small RNAs with big functions. Nat. Rev. Genet. 2019; 20: 89–108. PubMed Abstract | Publisher Full Text

[14] 14. Grimson A, Srivastava M, Fahey B, et al.: Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature. 2008; 455: 1193–1197. PubMed Abstract | Publisher Full Text | Free Full Text

Time-resolved small RNA transcriptomics of the ichthyosporean Sphaeroforma arctica

Abstract

Keywords

Introduction

Methods

Experimental design and culturing conditions and RNA extraction

Library preparation and sequencing details

Limitations

Data availability

Underlying data

Table 1. Overview of the data files.

Acknowledgements

References

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