Nucleotide diversity of functionally different groups of immune response genes in Old World camels based on newly annotated and reference-guided assemblies

- Nucleotide diversity of functionally different groups of immune response.
- Results: In this work, we improved the genome assemblies of the three Old World camel species – domestic dromedary and Bactrian camel, and the two-humped wild camel – via different computational methods.
- These upgraded assemblies were then used to assess nucleotide diversity of IR genes within and between species, and to compare the diversity found in immune genes and the rest of the genes in the genome.
- We detected differences in the nucleotide diversity among the three Old World camelid species and between IR gene groups, i.e., innate versus adaptive.
- Among the three species, domestic Bactrian camels showed the highest mean nucleotide diversity.
- Among the functionally different IR gene groups, the highest mean nucleotide diversity was observed in the major histocompatibility complex..
- ferus genome assembly from Ming et al., [12].
- Mean coverage throughout the genomes of the three Old World camel species was not different among spe- cies (F P = 0.8307.
- These results are in accordance with what was found in Fitak et al.
- although in Jirimutu et al.
- Nucleotide diversity among Old World camels in immune response and intra-genic regions.
- After improving the three Old World camel genome assemblies, we assessed the nucleotide diversity in im- mune response and intra-genic (within gene) regions..
- When looking at non-synonymous and synonymous SNPs and indels altogether, mean nucleotide diversity was found not to differ significantly for adaptive, in- nate IR genes and the rest-of-genome genes, but to be higher in MHC class I and II genes in both drom- edaries and domestic Bactrian camels (Fig.
- On the other hand, in wild camels, mean nucleotide diversity was not significantly different across gene types.
- When comparing nucleotide diversity per gene class in species pairs, mean MHC nucleotide diversity did not differ significantly for domestic Bactrian camels and dromedaries, as well as for wild camels and dromedaries, but differed between wild and do- mestic Bactrian camels, with the latter showing higher nucleotide mean diversity (Supplemental Fig.
- Innate and adaptive IR gene nucleotide diversity was statistically different between domestic Bactrian camels and the other two species, but the same between dromedaries and wild camels, while again Bactrian camels had a higher mean nucleotide diversity.
- Rest-of-genome gene nucleotide diversity was also higher for the Bactrian camel and different between this and the other two camel species..
- In domestic Bactrian camels, mean nucleotide diversity was the same for adaptive, innate and the rest-of-genome genes, but different in MHC genes where it was the highest.
- On the other hand, in wild camels, all gene groups had statistically the same mean nucleotide diversity.
- For both MHC and adaptive IR genes, mean nucleotide diversity was the same among the three camel species (Supplemental Fig.
- For in- nate IR genes, Bactrian and wild camels had the same mean nucleotide diversities, whereas dromedaries had a different mean nucleotide diversity from the other camel species, but the same compared to wild camels.
- There were 46 identified single-domain heavy-chain immunoglobulin genes in the Camelus ferus assembly of Ming et al.
- Mean nucleotide diversity was not significantly different among dromedaries, domes- tic camels, or wild camels when using either align- ments made with all SNPs and indels or only non- synonymous SNPs (see Supplemental Table 2 and Supplemental Fig.
- Nucleotide diversity in important immune gene groups Old World camels are known to be resistant to serious infectious diseases that threaten other livestock species inhabiting the same geographical regions, although they Table 3 Means with 95% bootstrap confidence limits (CL, see Methods) of nucleotide diversity for alignments made with non- synonymous and synonymous SNPs and indels and only non-synonymous SNPs for: DROM (dromedary.
- As our data were not nor- mally distributed and could not be transformed to ap- proximate a normal distribution, we assessed differences in nucleotide diversity within species in different immune complexes of the genome by using a non- parametric bootstrapping method to estimate 95% confi- dence intervals of mean nucleotide diversity (Fig.
- Ac- cording to the 95% confidence intervals derived from non-parametric bootstrap tests of mean nucleotide di- versities, we observed that MHC (class I and II) genes had higher mean nucleotide diversity compared to all other gene groups, for two-humped camels, in both SNPs-indels and just non-synonymous SNPs analyses, and for dromedaries in SNP-indels analysis but not for only non-synonymous SNP analysis (Fig.
- Previous re- search by Plasil et al., [4] showed that MHC nucleotide diversity within the three Old World species was gener- ally low.
- Over- all, mean nucleotide diversity was never different when comparing innate and adaptive IR gene groups in all three species, in both SNPs-indels and non-synonymous SNPs analyses..
- When comparing nucleotide diversity among both two-humped camel species, wild camels had lower mean.
- nucleotide diversity for both SNP and indels and non- synonymous SNP analyses, except for the MHC class I and II genes and for adaptive genes with non- synonymous SNPs (Supplemental Fig.
- Moreover, in general, the domestic Bactrian camel had higher mean nucleotide diversity compared to the wild camel, except for the mean nucleotide diversity in adaptive genes with non-synonymous SNPs.
- Principally in dromedaries, according to Lado et al.
- [45] and Fitak et al.
- [21], long-term popula- tion bottlenecks were detected, which probably reduced the nucleotide diversity even more in this species.
- Our results suggest that the IR genes follow the same pattern of rest-of-the-genome genes where do- mestic Bactrian camels are more diverse throughout all classes of genes when compared to the endangered wild camel..
- We also assessed the nucleotide diversity of single- domain heavy-chain immunoglobulin genes in our data..
- For that, we lifted the 46 heavy-chain immunoglobulin gene annotations from the Ming et al.
- These lower numbers might be due to as- sembly quality as the contig (not scaffold) lengths are much longer in the Ming et al.
- More- over, mean nucleotide diversity among dromedaries, domestic camels, and wild camels were not significantly different when using either alignments made with all SNPs and indels or only non-synonymous SNPs.
- In Ming et al.
- Interestingly, the alpaca, one of the four New World camel species, is evolutionarily the most closely related species to the Old World camels.
- PBJelly as- sembly was polished with Pilon [51] employing the same trimmed and error-corrected Illumina short-insert se- quences used for the de novo assembly of CamDro1 by Fitak et al.
- To assess the quality of the new assembly, we aligned 10 sets of paired-end RNA-Seq reads (Alim et al., 2019) to the original assembly (CamDro1), to CamDro2, the new assem- bly (CamDro3), and to several controls: C.
- Two of the 12 replicates were rejected for insufficient quality.
- We followed the same procedure as Elbers et al., [11]..
- 2.1.0 [53] of dromedary RNA-Seq reads from Sequence Read Archive accession: SRP017619 and Alim et al.
- 3.0.2 (Simão et al., 2015) searching for Eukaroyota OrthoDB v.
- Reference-guided assembly of the domestic Bactrian and wild camel genomes.
- ferus genome assembly from Ming et al.
- Chromosomal synteny between the wild camel and dromedary was analyzed by Ming et al..
- Nucleotide diversity.
- Two comparisons of nucleotide diversity were made, (i) between functionally different gene groups within each species: innate immune response genes, adaptive im- mune response genes, MHC class I and II genes, and rest-of-genome genes, and (ii) between Old World camel species: domesticated dromedaries and Bactrian camels, and wild camels among gene groups..
- Finally, we calculated nucleotide diversity for en- tire gene sequence multiple sequence alignments (each species separately) using the R package Pegas’s “nuc.div”.
- 3.6.3 to test for differences in mean nucleotide diversity within species among gene groups.
- For this we compared the 95% confidence inter- vals of the mean estimated with the boot.ci function’s.
- “species” (dromedary, domestic Bactrian camel, or wild camel) and response variable “ nucleotide diversity ” (adap- tive, innate, MHC, or rest-of-genome genes).
- To assess the nucleotide diversity of single-domain heavy-chain IG genes in our data, we first downloaded the scaffold.fasta.gz (Ming et al.’s [12] Camelus ferus genome assembly) and IGH.gff (heavy-chain immuno- globulin gene annotations) from https://figshare.com/arti- cles/Data_from_Chromosome-level_assembly_of_wild_Bac- trian_camel_genome_reveals_organization_of_immune_.
- We repeated previous nucleotide diversity assessment steps as described above (see Nucleotide diversity) using the new lifted over annotations.
- and compared mean nucleotide diversity in heavy-chain immunoglobulin genes among dromedaries, domestic camels, and wild camels..
- Assembly statistics for the CamFer2 and the Camelus ferus genome (new-CamFer) assembly from Ming et al.
- Klopp, 2018) dot plot made with Minimap2 [68] whole-genome align- ment between CamFer2 and the Camelus ferus genome (new-CamFer) assembly from Ming et al., [12].
- wrote the first draft of the manuscript, J.P.E.
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