Novel Insights to Assess Climate Resilience in Goats Using a Holistic Approach of Skin-Based Advanced NGS Technologies
Abstract
:1. Introduction
2. Results
2.1. Simulation of Comfort and Heat-Stress Environment within the Climate Chambers
2.2. Hair Fiber Analysis
2.3. Hair Cortisol Estimation
2.4. Hair Follicle qPCR Analysis
2.5. Sweating Rate and Active Sweat Gland Estimation
2.6. Skin Histology
2.7. Infrared Thermography of Caprine Skin
2.8. Skin 16S rRNA V3-V4 Metagenomics
2.9. Skin Transcriptomics Analysis
2.10. Skin Bisulfite Sequencing
2.11. Linking Skin Transcriptomics and Epigenetics Analysis
3. Discussion
4. Materials and Methods
4.1. Location of the Study
4.2. Animal Details
4.3. Experimental Design
4.4. Hair Fiber Analysis
4.5. Hair Cortisol Estimation
4.6. Hair Follicle qPCR Analysis
4.7. Sweating Rate and Active Sweat Gland Estimation
4.8. Skin Histology
4.9. Infrared Thermography of Caprine Skin
4.10. Skin 16S rRNA V3-V4 Metagenomics
4.11. Skin Transcriptomics Analysis
4.12. Skin Bisulfite Sequencing
4.13. Statiscial Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sequence Availability
References
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Variable | Kanni Aadu | Kodi Aadu | |||
---|---|---|---|---|---|
KAC | KAH | KOC | KOH | ||
Hair characteristics | Fiber diameter (µm) | 68.00 ± 2.43 a | 64.33 ± 1.49 a | 82.93 ± 3.18 b | 84.24 ± 3.97 b |
p-value: 0.00 | |||||
Staple length (cm) | 3.77 ± 0.03 b | 3.53 ± 0.12 ab | 3.72 ± 0.27 b | 3.11 ± 0.17 a | |
p-value: 0.05 | |||||
Hair cortisol | Hair cortisol (ng/mL) | 6.89 ± 0.16 a | 6.67 ± 0.16 a | 6.92 ± 0.22 a | 6.62 ± 0.16 a |
p-value: 0.54 | |||||
Hair follicle qPCR | HSP70 | 1.00 ± 0.08 a | 0.99 ± 0.12 a | 1.00 ± 0.13 a | 0.52 ± 0.19 b |
p-value: 0.89 | p-value: 0.02 | ||||
HSP90 | 1.00 ± 0.11 a | 0.63 ± 0.07 b | 1.00 ± 0.01 a | 0.26 ± 0.10 b | |
p-value: 0.01 | p-value: 0.00 | ||||
HSP110 | 1.00 ± 0.09 a | 0.98 ± 0.06 a | 1.00 ± 0.15 a | 0.68 ± 0.07 b | |
p-value: 0.81 | p-value: 0.05 | ||||
Sweating | Sweating rate (g/m2/h) | 0.00 ± 0.00 a | 2.80 ± 0.37 b | 0.00 ± 0.00 a | 2.82 ± 0.37 b |
p-value: 0.00 | |||||
Active sweat gland measurement (No of gland/cm2) | 0.00 ± 0.00 a | 0.03 ± 0.01 b | 0.00 ± 0.00 a | 0.06 ± 0.01 b | |
p-value: 0.00 | |||||
Skin histometry | Epithelial height (µm) | 15.62 ± 0.23 a | 16.84 ± 0.18 b | 18.15 ± 0.49 c | 22.94 ± 0.60 d |
p-value: 0.00 | |||||
No. of sweat glands/cm2 | 421.67 ± 3.53 a | 422.75 ± 1.83 ab | 429.33 ± 2.14 bc | 431.42 ± 1.97 c | |
p-value: 0.00 | |||||
Skin-surface infra-red thermal imaging | Eye (°C) | 36.93 ± 0.11 a | 40.96 ± 0.12 b | 36.88 ± 0.15 a | 41.14 ± 0.09 b |
p-value: 0.00 | |||||
Forehead (°C) | 29.39 ± 0.10 a | 40.44 ± 0.47 b | 29.83 ± 0.24 a | 40.28 ± 0.13 b | |
p-value: 0.00 | |||||
Flank (°C) | 30.68 ± 0.26 a | 40.78 ± 0.22 b | 31.34 ± 0.27 a | 40.43 ± 0.13 b | |
p-value: 0.00 | |||||
Back (°C) | 28.73 ± 0.47 a | 40.41 ± 0.16 c | 29.63 ± 0.24 b | 39.83 ± 0.13 a | |
p-value: 0.00 | |||||
Front leg (°C) | 27.06 ± 0.34 a | 40.71 ± 0.25 b | 27.30 ± 0.13 a | 40.38 ± 0.20 b | |
p-value: 0.00 | |||||
Skin 16S rRNA V3-V4 metagenomics | Relative abundance of microbes at phylum level (%) | ||||
Bacteroidetes | 31.86 | 33.23 | 37.10 | 31.38 | |
Firmicutes | 21.40 | 29.00 | 28.13 | 27.76 | |
Proteobacteria | 31.86 | 18.54 | 20.21 | 17.12 | |
Actinobacteria | 7.67 | 12.44 | 6.02 | 17.48 | |
Spirochaetes | 2.25 | 2.27 | 2.52 | 1.58 | |
Fibrobacteres | 2.40 | 1.04 | 1.68 | 1.56 | |
Verrucomicrobia | 1.26 | 1.52 | 2.30 | 1.49 | |
TM7 | 0.61 | 1.23 | 1.04 | 0.69 |
Hair Characteristics | Hair Cortisol | Hair Follicle qPCR | Sweating | Skin Histometry | Skin-Surface Infra-Red Thermal Imaging | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Breed | Group | THI | FD | SL | HCC | HSP70 | HSP90 | HSP110 | SR | ASG | SEH | SG | Eye | FH | Back | Flank | L | |
Breed | 1 | |||||||||||||||||
Group | 0.89 ** | 1 | ||||||||||||||||
THI | 0.00 | 0.45 * | 1 | |||||||||||||||
FD | 0.79 ** | 0.69 ** | −0.05 | 1 | ||||||||||||||
SL | −0.26 | −0.43 * | −0.46 * | −0.27 | 1 | |||||||||||||
HCC | −0.01 | −0.15 | −0.31 | 0.23 | 0.01 | 1 | ||||||||||||
HSP70 | 0.84 ** | 0.90 ** | 0.34 | 0.68 ** | −0.43 * | −0.05 | 1 | |||||||||||
HSP90 | 0.74 ** | 0.93 ** | 0.60 ** | 0.58 ** | −0.52 ** | −0.25 | 0.91 ** | 1 | ||||||||||
HSP110 | 0.86 ** | 0.91 ** | 0.31 | 0.76 ** | −0.35 | −0.13 | 0.91 ** | 0.91 ** | 1 | |||||||||
SR | 0.00 | 0.44 * | 0.99 ** | −0.07 | −0.44 * | −0.34 | 0.34 | 0.60 ** | 0.31 | 1 | ||||||||
ASG | 0.20 | 0.55 ** | 0.82 ** | 0.23 | −0.59 ** | −0.25 | 0.50 * | 0.72 ** | 0.48 * | 0.83 ** | 1 | |||||||
SEH | 0.69 ** | 0.83 ** | 0.48 * | 0.58 ** | −0.45 * | −0.175 | 0.78 ** | 0.88 ** | 0.83 ** | 0.47 * | 0.51 * | 1 | ||||||
SG | 0.57 ** | 0.56 ** | 0.11 | 0.38 | −0.30 | −0.19 | 0.59 ** | 0.49 * | 0.55 ** | 0.12 | 0.14 | 0.41 * | 1 | |||||
Eye | 0.02 | 0.46 * | 0.99 ** | −0.02 | −0.45 * | −0.28 | 0.37 | 0.62 ** | 0.33 | 0.97 ** | 0.83 ** | 0.49 * | 0.12 | 1 | ||||
FH | 0.01 | 0.46 * | 0.99 ** | −0.04 | −0.47 * | −0.34 | 0.34 | 0.60 ** | 0.30 | 0.98 ** | 0.83 ** | 0.49 * | 0.1 | 0.99 ** | 1 | |||
B | 0.01 | 0.46 * | 0.99 ** | −0.02 | −0.42 * | −0.28 | 0.33 | 0.59 ** | 0.29 | 0.98 ** | 0.87 ** | 0.47 * | 0.09 | 0.99 ** | 0.99 ** | 1 | ||
Flank | 0.02 | 0.46 * | 0.99 ** | −0.02 | −0.42 * | −0.29 | 0.34 | 0.59 ** | 0.31 | 0.98 ** | 0.82 ** | 0.48 * | 0.06 | 0.99 ** | 0.99 ** | 0.997 ** | 1 | |
L | −0.00 | 0.44 * | 0.997 ** | −0.04 | −0.45 * | −0.31 | 0.33 | 0.59 ** | 0.3 | 0.98 ** | 0.82 ** | 0.48 * | 0.10 | 0.99 ** | 0.995 ** | 0.99 ** | 0.99 ** | 1 |
Variable | Kanni Aadu (KAC vs. KAH) | Kodi Aadu (KOC vs. KOH) | |
---|---|---|---|
Skin transcriptomics | DEGs | 7993 | 2036 |
Up-regulated DEGs | 4237 | 302 | |
Down-regulated DEGs | 3756 | 1734 | |
Skin whole-genome bisulfite sequencing | DMR | 50,560 | 40,648 |
Hyper-methylated DMR | 25,178 | 19,657 | |
Hypo-methylated DMR | 25,382 | 20,991 | |
DMG | 14,646 | 13,388 | |
Hyper-methylated DMG | 7336 | 6507 | |
Hypo-methylated DMG | 7310 | 6904 |
KAC_vs_KAH | KOC_vs_KOH | ||
---|---|---|---|
Gene | Log2FC | Gene | Log2FC |
EIF–ATF pathway | |||
EIF2A | 1.775 | ||
EIF2B1 | −1.343 | ||
EIF2B2 | 1.398 | ||
EIF2B4 | 2.026 | EIF2B4 | −1.337 |
EIF2B5 | 1.547 | EIF2B5 | −1.77 |
EIF2S1 | 1.702 | ||
EIF2S2 | −1.416 | ||
EIF2S3 | 1.752 | EIF2S3 | −1.493 |
ATF4 | 2.369 | ATF4 | −1.875 |
ATF5 | 2.519 | ATF5 | −1.367 |
Stress-associated molecular chaperones | |||
UBQLN2 | 1.593 | UBQLN2 | −1.437 |
UBQLN3 | −7.974 | ||
HSF1 | 2.078 | ||
HSP70.1 | 3.035 | HSP70.1 | −1.492 |
HSP90AB1 | 2.285 | ||
HSP90B1 | 1.863 | HSP90B1 | −1.392 |
HSBP1L1 | −2.111 | ||
HSPA13 | −1.108 | ||
HSPA14 | −1.344 | ||
HSPA4 | −1.1 | ||
HSPA5 | 2.021 | HSPA5 | −1.591 |
HSPA8 | 2.098 | HSPA8 | −1.756 |
HSPA9 | 1.805 | ||
HSPB1 | 4.01 | HSPB1 | −1.898 |
HSPB3 | −2.07 | ||
HSPB6 | 3.04 | HSPB6 | −1.665 |
HSPB8 | 2.799 | HSPB8 | −1.901 |
HSPBP1 | 1.771 | ||
HSPD1 | 1.555 |
KAC_vs_KAH | KOC_vs_KOH | ||||
---|---|---|---|---|---|
Description | No. of DEG | p-Value | Description | No. of DEG | p-Value |
Metabolic pathways | 499 | 0.00 | Metabolic pathways | 189 | 0.00 |
Neuroactive ligand–receptor interaction | 124 | 0.00 | Huntington’s disease | 64 | 0.00 |
Ribosome | 113 | 0.00 | Oxidative phosphorylation | 62 | 0.00 |
Huntington’s disease | 109 | 0.00 | Parkinson’s disease | 61 | 0.00 |
Biosynthesis of antibiotics | 105 | 0.00 | Alzheimer’s disease | 58 | 0.00 |
Endocytosis | 97 | 0.02 | Biosynthesis of antibiotics | 51 | 0.00 |
Parkinson’s disease | 93 | 0.00 | Spliceosome | 35 | 0.00 |
Oxidative phosphorylation | 90 | 0.00 | Endocytosis | 34 | 0.03 |
Protein processing in endoplasmic reticulum | 81 | 0.00 | RNA transport | 28 | 0.01 |
Spliceosome | 77 | 0.00 | Protein processing in endoplasmic reticulum | 28 | 0.01 |
RNA transport | 71 | 0.01 | Carbon metabolism | 24 | 0.00 |
Lysosome | 54 | 0.02 | Proteasome | 23 | 0.00 |
Carbon metabolism | 53 | 0.01 | Lysosome | 22 | 0.01 |
Epstein–Barr virus infection | 48 | 0.05 | Cardiac muscle contraction | 20 | 0.00 |
Retrograde endocannabinoid signaling | 44 | 0.05 | Ribosome biogenesis in eukaryotes | 18 | 0.00 |
Antigen processing and presentation | 41 | 0.00 | Biosynthesis of amino acids | 16 | 0.00 |
Cardiac muscle contraction | 41 | 0.00 | Pyrimidine metabolism | 16 | 0.04 |
GABAergic synapse | 41 | 0.01 | Glutathione metabolism | 11 | 0.02 |
Proteasome | 37 | 0.00 | Citrate cycle (TCA cycle) | 9 | 0.01 |
Biosynthesis of amino acids | 36 | 0.01 | Pyruvate metabolism | 9 | 0.03 |
Bile secretion | 36 | 0.02 | RNA polymerase | 8 | 0.02 |
Arginine and proline metabolism | 29 | 0.00 | Steroid biosynthesis | 7 | 0.02 |
Fat digestion and absorption | 27 | 0.00 | |||
Glutathione metabolism | 26 | 0.01 | |||
Ether lipid metabolism | 23 | 0.04 | |||
Phototransduction | 17 | 0.00 | |||
alpha-Linolenic acid metabolism | 16 | 0.02 | |||
RNA polymerase | 16 | 0.04 | |||
Citrate cycle (TCA cycle) | 16 | 0.05 |
Group | Total Reads | QC Passed Reads | % Mapped Reads | % Methylated Cs | % Methylated CpG | % Methylated CHG | % Methylated CHH |
---|---|---|---|---|---|---|---|
KAC | 49,128,009 | 48,056,118 | 50.35 | 5.97 | 85.54 | 3.34 | 11.12 |
KAH | 54,655,288 | 53,458,502 | 52.66 | 5.90 | 85.71 | 3.22 | 11.07 |
KOC | 56,831,837 | 55,694,741 | 52.21 | 5.69 | 84.84 | 3.40 | 11.75 |
KOH | 48,747,713 | 47,743,401 | 51.62 | 5.61 | 85.03 | 3.32 | 11.65 |
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Mullakkalparambil Velayudhan, S.; Sejian, V.; Devaraj, C.; Manjunathareddy, G.B.; Ruban, W.; Kadam, V.; König, S.; Bhatta, R. Novel Insights to Assess Climate Resilience in Goats Using a Holistic Approach of Skin-Based Advanced NGS Technologies. Int. J. Mol. Sci. 2023, 24, 10319. https://doi.org/10.3390/ijms241210319
Mullakkalparambil Velayudhan S, Sejian V, Devaraj C, Manjunathareddy GB, Ruban W, Kadam V, König S, Bhatta R. Novel Insights to Assess Climate Resilience in Goats Using a Holistic Approach of Skin-Based Advanced NGS Technologies. International Journal of Molecular Sciences. 2023; 24(12):10319. https://doi.org/10.3390/ijms241210319
Chicago/Turabian StyleMullakkalparambil Velayudhan, Silpa, Veerasamy Sejian, Chinnasamy Devaraj, Gundallahalli Bayyappa Manjunathareddy, Wilfred Ruban, Vinod Kadam, Sven König, and Raghavendra Bhatta. 2023. "Novel Insights to Assess Climate Resilience in Goats Using a Holistic Approach of Skin-Based Advanced NGS Technologies" International Journal of Molecular Sciences 24, no. 12: 10319. https://doi.org/10.3390/ijms241210319