The genome of the extremophile Artemia provides insight into strategies to cope with extreme environments
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Date
Authors
De Vos, Stephanie
Rombauts, Stephane
Coussement, Louis
Dermauw, Wannes
Vuylsteke, Marnik
Sorgeloos, Patrick
Clegg, James S.
Nambu, Ziro
Van Nieuwerburgh, Filip
Norouzitallab, Parisa
Journal Title
Journal ISSN
Volume Title
Publisher
BMC
Abstract
BACKGROUND : Brine shrimp Artemia have an unequalled ability to endure extreme salinity and complete anoxia. This
study aims to elucidate its strategies to cope with these stressors.
RESULTS AND DISCUSSION : Here, we present the genome of an inbred A. franciscana Kellogg, 1906. We identified
21,828 genes of which, under high salinity, 674 genes and under anoxia, 900 genes were differentially expressed
(42%, respectively 30% were annotated). Under high salinity, relevant stress genes and pathways included several
Heat Shock Protein and Leaf Embryogenesis Abundant genes, as well as the trehalose metabolism. In addition, based
on differential gene expression analysis, it can be hypothesized that a high oxidative stress response and
endocytosis/exocytosis are potential salt management strategies, in addition to the expression of major facilitator
superfamily genes responsible for transmembrane ion transport. Under anoxia, genes involved in mitochondrial
function, mTOR signalling and autophagy were differentially expressed. Both high salt and anoxia enhanced
degradation of erroneous proteins and protein chaperoning. Compared with other branchiopod genomes, Artemia
had 0.03% contracted and 6% expanded orthogroups, in which 14% of the genes were differentially expressed
under high salinity or anoxia. One phospholipase D gene family, shown to be important in plant stress response,
was uniquely present in both extremophiles Artemia and the tardigrade Hypsibius dujardini, yet not differentially
expressed under the described experimental conditions.
CONCLUSIONS : A relatively complete genome of Artemia was assembled, annotated and analysed, facilitating
research on its extremophile features, and providing a reference sequence for crustacean research.
Description
Additional file 1. Assembly characteristics of all assembled crustacean
genomes. Characteristics listed are: species, whether the species genome
is annotated yes or no, N50 of the fragments with the highest assembly
hierarchy, number of fragments with the highest assembly hierarchy in
the assembly, haploid genome size, assembly size, completeness of the
assembly (=haploid GS/assembly size), taxonomic lineage (NCBI
taxonomy), reference for the genome paper.
Additional file 2. Evolution of Artemia assembly quality metrics throughout the assembly steps. Evolution of the scaffold N50, the number of fragments and the genome completeness (assembly size/ genome size) in the subsequent Artemia assembly stages
Additional file 3 BUSCO analysis results for the A. franciscana genome assembly and annotation.
Additional file 4. BLAST results for mitochondrial genes in the Artemia genome. Listed: Query accession and gene name, presence of a (significant) BLAST hit in the Artemia proteome with the highest bit score, E-value and bit score of the hit, scaffold length of the scaffold on which the hit lies, percentage of mitochondrial genes on this scaffold.
Additional file 5. Taxonomic groups of alien genomes identified in the Artemia genome.
Additional file 6 Expanded or contracted Artemia orthogroups compared to other Branchiopoda. Listed: Orthogroup ID, number of genes in this orthogroup in A. franciscana, D. pulex, L. arcticus, and E. texana, expanded or contracted status of the orthogroup in Artemia compared to D. pulex, L. arcticus and E. texana, conservation in Branchiopoda (whether this orthogroup contains genes for each branchiopod), comma-separated IPR description of Artemia genes in this orthogroup, Artemia genes in this orthogroup.
Additional file 7 GO enrichment of Artemia compared to other Branchiopoda. Listed: GO ID, name and category, false discovery rate (FDR) and P value of the Fisher’s exact test enrichment analysis in Blast2GO, number of Artemia genes from expanded/contracted orthogroups in this GO ID, number of whole Artemia genome genes in this GO category, number of Artemia genes from expanded/contracted orthogroups in this GO ID without GO annotation. The Fisher’s Exact Test is sensitive in the direction of the test: the genes that are present in the test-set and also in the reference genome set will be deleted from the reference, but not from the test set, resulting in zero sequences in the reference set and values above zero in the test set. Significantly enriched GOs (FDR ≤ 0.05, biological process) of Artemia genes in expanded or contracted orthogroups compared to Branchiopoda are given.
Additional file 8 Expanded or contracted Artemia and H. dujardini orthogroups compared to other Arthropoda. Listed: Orthogroup ID, number of genes in this orthogroup in A. franciscana and in the other arthropod species, expanded or contracted status of the orthogroup in Artemia compared to the other arthropod species, comma-separated IPR description of Artemia genes in this orthogroup, H. dujardini genes in this orthogroup, Artemia genes in this orthogroup.
Additional file 9. STAR mapping statistics for differential expression analysis in Artemia. Listed: sample name, total number of reads for this sample, percentage of uniquely mapped reads, absolute number of uniquely mapped reads, percentage of multi mapped reads, absolute number of multi mapped reads.
Additional file 10. Summarization statistics for differential expression analysis in Artemia. Listed: sample name, total counts, percentage of counts assigned to a gene annotation, absolute counts assigned to a gene annotation. * notice that this amount can be more than the sum of uniquely mapped + multi-mapped in the mapping statistics since multimapped reads are considered.
Additional file 11 Differentially expressed genes under high salinity (p < 0.05). Listed: functional annotation of the differentially expressed gene, gene ID in the genome annotation and on the ORCAE platform, p value, average log fold change of gene expression under high salinity, gene regulation of the differentially expressed gene (up or down), InterPro description of the gene family to which the gene belongs.
Additional file 12 Differentially expressed genes under anoxia (p < 0.05). Listed: functional annotation of the differentially expressed gene, gene ID in the genome annotation and on the ORCAE platform, p value, log fold change of gene expression under anoxia, gene regulation of the differentially expressed gene (up or down), InterPro description of the gene family to which the gene belongs.
Additional file 13 GO enrichment in Artemia under high salinity. Significantly Enriched GOs (FDR ≤ 0.05) of Artemia genes differentially expressed under high salinity. Listed: GO ID, name and category, false discovery rate (FDR) and P value of the Fisher’s exact test enrichment analysis in Blast2GO, number of DEG under high salinity in this GO category, number of whole Artemia genome genes in this GO category, number of DEG under high salinity without GO annotation. The Fisher’s Exact Test is sensitive in the direction of the test: the genes that are present in the test-set and also in the reference genome set will be deleted from the reference, but not from the test set, resulting in zero sequences in the reference set and values above zero in the test set.
Additional file 14 Pathway enrichment in Artemia under high salinity. Significantly enriched (Fisher’s exact test corrected for multiple testing, FDR ≤ 0.05) pathways of Artemia genes differentially expressed under high salinity. Listed in first worksheet (STRING annotation): gene number, ORCAE gene ID, STRING Daphnia pulex gene ID, BLAST identity and bit score, gene name and gene annotation. Listed in second worksheet (STRING pathway enrichment): KEGG Daphnia pulex pathway name, pathway description, number of DEG under high salinity in this pathway, number of genes in the D. pulex genome that belong to this pathway, enrichment FDR, matching D. pulex gene IDs, matching gene names in pathways shown in figures and additional files, matching D. pulex gene ID labels.
Additional file 15. Consolidation of DEG analysis, GO enrichment and pathway enrichment in Artemia under high salinity.
Additional file 16. The enriched Carbon metabolism pathway in Artemia under high salinity. Up- and downregulated genes are indicated on the KEGG map dpx01200.
Additional file 17. GO enrichment in Artemia under anoxia. Significantly enriched GOs (FDR ≤ 0.05) of Artemia genes differentially expressed under anoxia. Listed: GO ID, name and category, false discovery rate (FDR) and P value of the Fisher’s exact test enrichment analysis in Blast2GO, number of DEG under anoxia in this GO ID, number of whole Artemia genome genes in this GO ID, number of DEG under anoxia without GO annotation. The Fisher’s Exact Test is sensitive in the direction of the test: the genes that are present in the test set and also in the reference genome set will be deleted from the reference, but not from the test set, resulting in zero sequences in the reference set and values above zero in the test set.
Additional file 18 Pathway enrichment in Artemia under anoxia. Significantly enriched (Fisher’s exact test corrected for multiple testing, FDR ≤ 0.05) pathways of Artemia genes differentially expressed under anoxia. Listed in first worksheet (STRING annotation): gene number, ORCAE gene ID, STRING Daphnia pulex gene ID, BLAST identity and bit score, gene name and gene annotation. Listed in second worksheet (STRING pathway enrichment): KEGG Daphnia pulex pathway name, pathway description, number of DEG under anoxia in this pathway, number of genes in the D. pulex genome that belong to this pathway, enrichment FDR, matching D. pulex gene IDs, matching gene names in pathways shown in figures and additional files, matching D. pulex gene ID labels.
Additional file 19. Consolidation of DEG analysis, GO enrichment and pathway enrichment in Artemia under anoxia.
Additional file 20. The enriched N-glycan biosynthesis pathway in Artemia under anoxia. Up- and downregulated genes are indicated on the KEGG map dpx00510.
Additional file 21. The enriched Basal transcription factors pathway in Artemia under anoxia. Up- and downregulated genes are indicated on the KEGG map dpx03022.
Additional file 22. Augustus custom training files for Artemia. Includes probabilities, parameters and weights used for Augustus training for annotation of the Artemia genome.
Additional file 23. EuGene custom parameter file for Artemia. Includes parameters used for EuGene training for annotation of the Artemia genome.
Additional file 24. Sequence GC-content profiles for all samples used for differential expression analysis.
Additional file 2. Evolution of Artemia assembly quality metrics throughout the assembly steps. Evolution of the scaffold N50, the number of fragments and the genome completeness (assembly size/ genome size) in the subsequent Artemia assembly stages
Additional file 3 BUSCO analysis results for the A. franciscana genome assembly and annotation.
Additional file 4. BLAST results for mitochondrial genes in the Artemia genome. Listed: Query accession and gene name, presence of a (significant) BLAST hit in the Artemia proteome with the highest bit score, E-value and bit score of the hit, scaffold length of the scaffold on which the hit lies, percentage of mitochondrial genes on this scaffold.
Additional file 5. Taxonomic groups of alien genomes identified in the Artemia genome.
Additional file 6 Expanded or contracted Artemia orthogroups compared to other Branchiopoda. Listed: Orthogroup ID, number of genes in this orthogroup in A. franciscana, D. pulex, L. arcticus, and E. texana, expanded or contracted status of the orthogroup in Artemia compared to D. pulex, L. arcticus and E. texana, conservation in Branchiopoda (whether this orthogroup contains genes for each branchiopod), comma-separated IPR description of Artemia genes in this orthogroup, Artemia genes in this orthogroup.
Additional file 7 GO enrichment of Artemia compared to other Branchiopoda. Listed: GO ID, name and category, false discovery rate (FDR) and P value of the Fisher’s exact test enrichment analysis in Blast2GO, number of Artemia genes from expanded/contracted orthogroups in this GO ID, number of whole Artemia genome genes in this GO category, number of Artemia genes from expanded/contracted orthogroups in this GO ID without GO annotation. The Fisher’s Exact Test is sensitive in the direction of the test: the genes that are present in the test-set and also in the reference genome set will be deleted from the reference, but not from the test set, resulting in zero sequences in the reference set and values above zero in the test set. Significantly enriched GOs (FDR ≤ 0.05, biological process) of Artemia genes in expanded or contracted orthogroups compared to Branchiopoda are given.
Additional file 8 Expanded or contracted Artemia and H. dujardini orthogroups compared to other Arthropoda. Listed: Orthogroup ID, number of genes in this orthogroup in A. franciscana and in the other arthropod species, expanded or contracted status of the orthogroup in Artemia compared to the other arthropod species, comma-separated IPR description of Artemia genes in this orthogroup, H. dujardini genes in this orthogroup, Artemia genes in this orthogroup.
Additional file 9. STAR mapping statistics for differential expression analysis in Artemia. Listed: sample name, total number of reads for this sample, percentage of uniquely mapped reads, absolute number of uniquely mapped reads, percentage of multi mapped reads, absolute number of multi mapped reads.
Additional file 10. Summarization statistics for differential expression analysis in Artemia. Listed: sample name, total counts, percentage of counts assigned to a gene annotation, absolute counts assigned to a gene annotation. * notice that this amount can be more than the sum of uniquely mapped + multi-mapped in the mapping statistics since multimapped reads are considered.
Additional file 11 Differentially expressed genes under high salinity (p < 0.05). Listed: functional annotation of the differentially expressed gene, gene ID in the genome annotation and on the ORCAE platform, p value, average log fold change of gene expression under high salinity, gene regulation of the differentially expressed gene (up or down), InterPro description of the gene family to which the gene belongs.
Additional file 12 Differentially expressed genes under anoxia (p < 0.05). Listed: functional annotation of the differentially expressed gene, gene ID in the genome annotation and on the ORCAE platform, p value, log fold change of gene expression under anoxia, gene regulation of the differentially expressed gene (up or down), InterPro description of the gene family to which the gene belongs.
Additional file 13 GO enrichment in Artemia under high salinity. Significantly Enriched GOs (FDR ≤ 0.05) of Artemia genes differentially expressed under high salinity. Listed: GO ID, name and category, false discovery rate (FDR) and P value of the Fisher’s exact test enrichment analysis in Blast2GO, number of DEG under high salinity in this GO category, number of whole Artemia genome genes in this GO category, number of DEG under high salinity without GO annotation. The Fisher’s Exact Test is sensitive in the direction of the test: the genes that are present in the test-set and also in the reference genome set will be deleted from the reference, but not from the test set, resulting in zero sequences in the reference set and values above zero in the test set.
Additional file 14 Pathway enrichment in Artemia under high salinity. Significantly enriched (Fisher’s exact test corrected for multiple testing, FDR ≤ 0.05) pathways of Artemia genes differentially expressed under high salinity. Listed in first worksheet (STRING annotation): gene number, ORCAE gene ID, STRING Daphnia pulex gene ID, BLAST identity and bit score, gene name and gene annotation. Listed in second worksheet (STRING pathway enrichment): KEGG Daphnia pulex pathway name, pathway description, number of DEG under high salinity in this pathway, number of genes in the D. pulex genome that belong to this pathway, enrichment FDR, matching D. pulex gene IDs, matching gene names in pathways shown in figures and additional files, matching D. pulex gene ID labels.
Additional file 15. Consolidation of DEG analysis, GO enrichment and pathway enrichment in Artemia under high salinity.
Additional file 16. The enriched Carbon metabolism pathway in Artemia under high salinity. Up- and downregulated genes are indicated on the KEGG map dpx01200.
Additional file 17. GO enrichment in Artemia under anoxia. Significantly enriched GOs (FDR ≤ 0.05) of Artemia genes differentially expressed under anoxia. Listed: GO ID, name and category, false discovery rate (FDR) and P value of the Fisher’s exact test enrichment analysis in Blast2GO, number of DEG under anoxia in this GO ID, number of whole Artemia genome genes in this GO ID, number of DEG under anoxia without GO annotation. The Fisher’s Exact Test is sensitive in the direction of the test: the genes that are present in the test set and also in the reference genome set will be deleted from the reference, but not from the test set, resulting in zero sequences in the reference set and values above zero in the test set.
Additional file 18 Pathway enrichment in Artemia under anoxia. Significantly enriched (Fisher’s exact test corrected for multiple testing, FDR ≤ 0.05) pathways of Artemia genes differentially expressed under anoxia. Listed in first worksheet (STRING annotation): gene number, ORCAE gene ID, STRING Daphnia pulex gene ID, BLAST identity and bit score, gene name and gene annotation. Listed in second worksheet (STRING pathway enrichment): KEGG Daphnia pulex pathway name, pathway description, number of DEG under anoxia in this pathway, number of genes in the D. pulex genome that belong to this pathway, enrichment FDR, matching D. pulex gene IDs, matching gene names in pathways shown in figures and additional files, matching D. pulex gene ID labels.
Additional file 19. Consolidation of DEG analysis, GO enrichment and pathway enrichment in Artemia under anoxia.
Additional file 20. The enriched N-glycan biosynthesis pathway in Artemia under anoxia. Up- and downregulated genes are indicated on the KEGG map dpx00510.
Additional file 21. The enriched Basal transcription factors pathway in Artemia under anoxia. Up- and downregulated genes are indicated on the KEGG map dpx03022.
Additional file 22. Augustus custom training files for Artemia. Includes probabilities, parameters and weights used for Augustus training for annotation of the Artemia genome.
Additional file 23. EuGene custom parameter file for Artemia. Includes parameters used for EuGene training for annotation of the Artemia genome.
Additional file 24. Sequence GC-content profiles for all samples used for differential expression analysis.
Keywords
Arthropod, Genome, Transcriptome, Assembly, Annotation, Extremophile, Salinity, Anoxia, Artemia, Brine shrimp
Sustainable Development Goals
Citation
De Vos, S., Rombauts, S., Coussement, L. et al. 2021, 'The genome of the extremophile Artemia provides insight into strategies to cope with extreme environments', BMC Genomics, vol. 22, art. 635, pp. 1-26.