Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sample Collection
2.2. Experimental Design
2.3. Physiological Assessment
2.3.1. Microelectrode Measurements
2.3.2. Holobiont Mortality and Growth
2.3.3. Color and Chlorophyll a
2.3.4. Test Surface, Pore Size and Breakage
2.3.5. Statistics
2.4. Identification of Photosymbionts
2.5. Proteomics
2.5.1. Label-Free Peptide Quantification and Protein Identification
2.5.2. Differential Protein Abundance and Functional Annotations
3. Results
3.1. Physicochemical Parameters of Seawater Treatments
3.2. Identification of Photosymbionts
3.3. Physiological Assessments of Holobiont and Photosymbiont Condition
3.3.1. Microelectrode Measurements
3.3.2. Color and Chlorophyll a
3.3.3. Holobiont Mortality and Growth
3.3.4. Test Surface, Pore Size and Breakage
3.4. Proteomics
3.4.1. Label-Free Peptide Quantification and Protein Identification
3.4.2. Differential Abundant Protein (DAP) Distribution in Treatments and Compartments
3.4.3. Functional Categories of Photosymbiont- and Host-Associated DAPs
4. Discussion
4.1. Climate Change Impacts on Photosymbiont and Holobiont Performance
4.1.1. Bleaching and Mortality
4.1.2. Growth
4.2. Buffering of OA in the LBF Microenvironment
4.3. Non-Linear Responses to Multiple Climate Change Stressors
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
Proteomics Analysis
References
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Treatment | T (°C) | DIC (µM) | TA (µM) | pHSW | pCO2 (ppm) | ΩC | ΩA |
---|---|---|---|---|---|---|---|
C28 | 28.2 ± 0.2 | 2562 ± 288 | 2928 ± 280 | 8.21 ± 0.10 | 483 ± 86 | 8.5 ± 1.2 | 5.5 ± 1.2 |
C31 | 31.0 ± 0.6 | 2375 ± 283 | 2738 ± 278 | 8.11 ± 0.13 | 500 ± 74 | 8.1 ± 1.3 | 4.8 ± 1.2 |
M28 | 28.0 ± 0.1 | 2686 ± 285 | 2937 ± 258 | 7.95 ± 0.07 | 973 ± 138 | 5.9 ± 2.6 | 3.7 ± 1.9 |
M31 | 30.9 ± 0.2 | 2806 ± 254 | 3088 ± 233 | 7.98 ± 0.07 | 953 ± 131 | 6.6 ± 0.5 | 4.2 ± 0.6 |
H28 | 28.0 ± 0.2 | 2858 ± 430 | 2908 ± 456 | 7.49 ± 0.11 | 2934 ± 898 | 2.3 ± 0.4 | 1.4 ± 0.4 |
H31 | 30.9 ± 0.1 | 3231 ± 281 | 3294 ± 324 | 7.50 ± 0.10 | 3431 ± 810 | 2.9 ± 0.4 | 1.8 ± 0.5 |
Proteins | DF | MS | F | Pr (>F) | Post-Hoc Test Summary |
---|---|---|---|---|---|
Holobiont | |||||
pCO2 | 2 | 0.0003 | 1.818 | 0.028 | H:C 0.480, M:C 0.290, H:M 0.130 |
Temp. | 1 | 0.0004 | 2.335 | 0.013 | 31 °C:28 °C 0.080 |
pCO2×Temp. | 1 | 0.0003 | 1.719 | 0.075 | |
Foraminifera | |||||
pCO2 | 2 | 0.0003 | 1.854 | 0.030 | H:C 0.390 M:C 0.270, H:M 0.170 |
Temp. | 1 | 0.0004 | 2.358 | 0.018 | 31 °C:28 °C 0.079 |
pCO2×Temp. | 1 | 0.0003 | 1.697 | 0.091 | |
Photosymbiont | |||||
pCO2 | 2 | 0.0004 | 1.775 | 0.030 | H:C 0.607, M:C 0.321, H:M 0.091 |
Temp. | 1 | 0.0005 | 2.324 | 0.011 | 31 °C:28 °C 0.089 |
pCO2×Temp. | 1 | 0.0004 | 1.734 | 0.067 |
Protein Description | Log2(Fold-Change) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
M31/ M28 | H31/ H28 | H28/ M28 | H31/ M31 | M31/ C31 | H31/ C31 | M31/ H28 | C31/ M28 | H31/ M28 | C31/ H28 | |
Light-harvesting and photosynthesis | ||||||||||
protein fucoxanthin chlorophyll a/c | −2.34 | −0.27 | 0.05 | 2.11 | −2.63 | −0.51 | −2.38 | 0.29 | −0.22 | 0.24 |
protein fucoxanthin chlorophyll a/c | −1.90 | 0.15 | −0.19 | 1.86 | −2.12 | −0.25 | −1.71 | 0.21 | −0.04 | 0.40 |
divinyl chlorophyllidea 8-vinyl-reduct. | −2.60 | 0.81 | −0.48 | 2.93 | −2.56 | 0.37 | −2.12 | −0.04 | 0.33 | 0.44 |
thylakoid lumenal 15.0 kDa protein 2 | −1.03 | −0.09 | −0.16 | 0.78 | −0.76 | 0.02 | −0.87 | −0.28 | −0.25 | −0.12 |
cytochrome b6/f complex subunit IV | −3.18 | −0.17 | −4.64 | −1.64 | 4.27 | 2.63 | 1.46 | −7.45 | −4.81 | −2.81 |
Metabolic and biosynthetic processes | ||||||||||
uroporphyrinogen decarboxylase | −4.78 | −2.04 | −0.75 | 1.99 | −3.61 | −1.62 | −4.03 | −1.16 | −2.79 | −0.41 |
fructose-bisphosphate aldolase | −2.03 | −0.51 | 0.11 | 1.63 | −2.28 | −0.65 | −2.14 | 0.25 | −0.40 | 0.14 |
demethylmenaquinone methyltransfer. | −2.36 | −0.71 | 0.11 | 1.75 | −2.24 | −0.49 | −2.46 | −0.12 | −0.60 | −0.22 |
3-isopropylmalate dehydrogenase | −2.94 | −0.52 | −0.51 | 1.90 | −1.56 | 0.34 | −2.43 | −1.38 | −1.04 | −0.87 |
glucose-6-phosphate isomerase | −1.14 | 0.47 | −0.09 | 1.53 | −1.08 | 0.44 | −1.05 | −0.05 | 0.39 | 0.03 |
cysteine desulfurase | −0.26 | 0.54 | 0.65 | 1.46 | −0.58 | 0.88 | −0.91 | 0.32 | 1.19 | −0.34 |
taurine catabolism dioxygenase TauD | −0.75 | −0.88 | −0.51 | −0.63 | −1.58 | −2.21 | −0.25 | 0.82 | −1.39 | 1.33 |
alanine dehydrogenase 2 | −1.00 | −0.43 | 0.03 | 0.60 | −0.47 | 0.12 | −1.03 | −0.52 | −0.40 | −0.55 |
inorganic pyrophosphatase | −0.72 | −0.44 | 0.30 | 0.58 | −0.61 | −0.03 | −1.02 | −0.12 | −0.14 | −0.41 |
inorganic pyrophosphatase | −0.79 | −0.63 | −0.03 | 0.13 | 0.00 | 0.13 | −0.76 | −0.79 | −0.66 | −0.76 |
phosphoadenosine-phosphosulphate red. | −0.36 | −1.08 | 0.27 | −0.45 | 0.11 | −0.33 | −0.63 | −0.47 | −0.81 | −0.75 |
S-adenosylmethionine synthase 2 | 0.65 | −0.25 | 0.20 | −0.70 | 1.03 | 0.33 | 0.45 | −0.38 | −0.05 | −0.58 |
geranylgeranyl reductase | 0.57 | −0.41 | −0.13 | −1.11 | 1.04 | −0.07 | 0.70 | −0.47 | −0.53 | −0.34 |
carbamoyl-phosphate synthase | −0.62 | −0.75 | −0.41 | −0.53 | −0.45 | −0.98 | −0.22 | −0.17 | −1.15 | 0.24 |
acetyl-coa carboxylase | −0.46 | −1.05 | −0.11 | −0.71 | −0.25 | −0.96 | −0.34 | −0.21 | −1.17 | −0.09 |
acetyl-coa carboxylase | −0.20 | −1.04 | −0.09 | −0.93 | −0.15 | −1.08 | −0.11 | −0.05 | −1.13 | 0.04 |
ALA dehydratase | −0.55 | −0.95 | −0.72 | −1.12 | 0.30 | −0.82 | 0.17 | −0.85 | −1.67 | −0.13 |
agmatinase | −1.54 | 0.40 | −1.19 | 0.75 | −0.10 | 0.65 | −0.35 | −1.44 | −0.79 | −0.24 |
glutamate synthase 2 [NADH] | −0.65 | −1.42 | −0.97 | −1.74 | 0.87 | −0.87 | 0.32 | −1.52 | −2.40 | −0.55 |
aspartate--ammonia ligase | 1.66 | 0.16 | 0.30 | −1.20 | 1.74 | 0.54 | 1.36 | −0.09 | 0.45 | −0.38 |
Proton transmembrane transport, cell redox homeostasis and cellular detoxification | ||||||||||
thioredoxin | −1.08 | 0.38 | −0.28 | 1.18 | −1.65 | −0.47 | −0.80 | 0.56 | 0.10 | 0.85 |
L-ascorbate peroxidase | −0.17 | −1.11 | 0.45 | −0.50 | 0.16 | −0.34 | −0.62 | −0.32 | −0.66 | −0.77 |
Protein folding, phosphorylation and transport | ||||||||||
translocation protein sec62 | −2.44 | 0.03 | −0.18 | 2.28 | −1.74 | 0.54 | −2.25 | −0.69 | −0.16 | −0.51 |
T-complex protein 1 subunit eta | −0.77 | 1.25 | 0.75 | 2.77 | −1.53 | 1.24 | −1.52 | 0.76 | 2.00 | 0.01 |
leucine-rich repeat-containing protein | 1.32 | 1.07 | 1.13 | 0.88 | −1.27 | −0.39 | 0.19 | 2.59 | 2.20 | 1.46 |
ATP-dependent chaperone ClpB | 1.29 | 0.12 | 0.34 | −0.83 | 0.84 | 0.00 | 0.95 | 0.46 | 0.46 | 0.11 |
luminal-binding protein 5 | 0.22 | −0.56 | −0.24 | −1.03 | 0.67 | −0.36 | 0.46 | −0.45 | −0.81 | −0.21 |
Proteolysis and autophagy | ||||||||||
Clp protease ATP binding subunit | 0.37 | −0.39 | −0.27 | −1.04 | 0.42 | −0.62 | 0.64 | −0.05 | −0.67 | 0.23 |
Translation and related process | ||||||||||
40S ribosomal protein | 0.24 | −0.72 | −0.52 | −1.49 | 0.76 | −0.73 | 0.77 | −0.51 | −1.24 | 0.01 |
Cytoskeleton and microtubule-based processes | ||||||||||
cell division protein FtsZ | −2.18 | 0.06 | −0.86 | 1.38 | −1.92 | −0.54 | −1.32 | −0.26 | −0.80 | 0.60 |
tubulin-specific chaperone d | −2.15 | −0.40 | −0.34 | 1.42 | −1.78 | −0.37 | −1.82 | −0.37 | −0.74 | −0.04 |
Unknown functions | ||||||||||
hypothetical protein | −1.54 | 0.78 | −1.74 | 0.57 | −0.64 | −0.06 | 0.21 | −0.90 | −0.96 | 0.84 |
Protein Description | Log2(Fold-Change) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
M31/ M28 | H31/ H28 | H28/ M28 | H31/ M31 | M31/ C31 | H31/ C31 | M31/ H28 | C31/ M28 | H31/ M28 | C31/ H28 | |
Signal transduction and regulation | ||||||||||
NEDD8-activating enzyme E1 regulat. | −2.34 | 0.42 | 0.35 | 3.11 | −3.08 | 0.03 | −2.69 | 0.74 | 0.77 | 0.39 |
cullin-associated NEDD8-dissociated 1 | −1.17 | 0.28 | 0.09 | 1.53 | −2.20 | −0.66 | −1.26 | 1.03 | 0.37 | 0.94 |
Ras-related protein Rab-21 | −1.08 | 0.55 | −0.15 | 1.48 | −1.76 | −0.27 | −0.93 | 0.68 | 0.40 | 0.83 |
GTPase HRas | −0.69 | 1.33 | 0.14 | 2.15 | −1.84 | 0.31 | −0.82 | 1.16 | 1.46 | 1.02 |
Ras-related protein Rab-7a-like | −1.37 | 0.74 | −0.83 | 1.28 | −1.34 | −0.05 | −0.55 | −0.04 | −0.09 | 0.79 |
cytochrome c oxidase assembly (SCO) | −1.12 | 0.32 | −0.28 | 1.15 | −0.92 | 0.23 | −0.84 | −0.20 | 0.03 | 0.09 |
guanine nucleotide-binding protein G | −1.11 | 0.35 | −0.96 | 0.50 | −0.79 | −0.29 | −0.15 | −0.32 | −0.61 | 0.63 |
Metabolic and biosynthetic processes | ||||||||||
long-chain-fatty-acid--CoA ligase | −5.28 | −0.68 | 1.28 | 5.88 | −5.41 | 0.47 | −6.56 | 0.13 | 0.60 | −1.15 |
aldo/keto reductase | −2.87 | −0.39 | −0.05 | 2.43 | −2.96 | −0.54 | −2.82 | 0.09 | −0.44 | 0.15 |
fructose-bisphosphate aldolase 6 | −1.47 | −0.19 | 0.19 | 1.47 | −1.65 | −0.18 | −1.66 | 0.18 | 0.00 | −0.01 |
glutathione S-transferase | −1.34 | 0.17 | −0.24 | 1.27 | −1.60 | −0.33 | −1.10 | 0.26 | −0.07 | 0.50 |
methylglutaconyl-CoA hydratase | −1.12 | −0.21 | −0.14 | 0.77 | −1.38 | −0.61 | −0.98 | 0.26 | −0.34 | 0.40 |
oligosaccharyltransferase complex | −1.33 | 0.39 | −0.12 | 1.59 | −1.01 | 0.58 | −1.20 | −0.32 | 0.27 | −0.19 |
putative glyoxalase I | −2.13 | −0.47 | −0.48 | 1.18 | −1.56 | −0.38 | −1.65 | −0.57 | −0.95 | −0.09 |
UDP-glucose 4-epimerase | −1.15 | −0.59 | 0.08 | 0.64 | −0.89 | −0.25 | −1.23 | −0.26 | −0.51 | −0.34 |
asparagine synthetase | −0.69 | 0.29 | −0.31 | 0.67 | −1.42 | −0.75 | −0.38 | 0.73 | −0.02 | 1.05 |
isocitrate dehydrogenase [NADP] | 0.08 | −0.65 | 0.72 | −0.02 | 0.39 | 0.37 | −0.64 | −0.31 | 0.06 | −1.02 |
cytochrome b-c1 complex subu. Rieske | −0.08 | −1.57 | 0.95 | −0.54 | 0.81 | 0.27 | −1.03 | −0.89 | −0.62 | −1.84 |
cytochrome c oxidase subunit 5b-1 | −0.17 | −1.25 | 0.43 | −0.65 | 0.57 | −0.08 | −0.60 | −0.74 | −0.82 | −1.17 |
2-oxoglutarate dehydrogenase | 0.17 | −1.08 | 0.35 | −0.90 | 0.70 | −0.20 | −0.18 | −0.53 | −0.73 | −0.88 |
adenylyl-sulfate kinase | 0.16 | −0.75 | −0.34 | −1.26 | 0.72 | −0.53 | 0.51 | −0.56 | −1.09 | −0.22 |
NADH dehydrogenase flavoprotein 1 | 0.89 | −0.80 | 0.72 | −0.97 | 1.09 | 0.12 | 0.17 | −0.20 | −0.08 | −0.92 |
phytanoyl-CoA dioxygenase | 1.12 | −0.40 | −0.10 | −1.61 | 1.37 | −0.24 | 1.22 | −0.25 | −0.49 | −0.15 |
fatty acyl-CoA synthetase | 0.97 | −0.34 | −0.23 | −1.55 | 1.57 | 0.02 | 1.20 | −0.60 | −0.58 | −0.37 |
UDP-glucose 4-epimerase GalE | 2.33 | −0.99 | 2.50 | −0.82 | 0.62 | −0.20 | −0.17 | 1.71 | 1.51 | −0.79 |
Proton transmembrane transport, cell redox homeostasis and cellular detoxification | ||||||||||
peroxiredoxin-1 | −1.28 | 0.57 | −0.73 | 1.13 | −0.40 | 0.73 | −0.56 | −0.88 | −0.15 | −0.15 |
Protein folding, phosphorylation and transport | ||||||||||
phage shock protein A homolog | −1.65 | 0.64 | −0.48 | 1.82 | −1.44 | 0.37 | −1.17 | −0.21 | 0.16 | 0.27 |
synaptobrevin domain-containing prot. | −0.09 | 0.89 | −0.78 | 0.20 | −0.62 | −0.42 | 0.69 | 0.54 | 0.12 | 1.31 |
CAMK/CDPK protein kinase | −0.07 | −0.13 | −1.20 | −1.27 | 0.51 | −0.76 | 1.13 | −0.58 | −1.33 | 0.62 |
sorting nexin 1 | 1.19 | −0.49 | 0.05 | −1.63 | 0.88 | −0.75 | 1.14 | 0.32 | −0.44 | 0.26 |
chaperone protein | 1.51 | 0.29 | 0.24 | −0.98 | 1.46 | 0.49 | 1.27 | 0.04 | 0.53 | −0.19 |
mitochondrial carrier family | −0.24 | −1.94 | 1.53 | −0.18 | −0.08 | −0.25 | −1.76 | −0.16 | −0.42 | −1.69 |
Proteolysis and autophagy | ||||||||||
oligopeptidase B | −2.93 | −2.72 | 0.02 | 0.23 | −1.85 | −1.62 | −2.95 | −1.08 | −2.70 | −1.10 |
ubiquitin carboxyl-terminal hydrolase | −0.42 | −0.41 | 0.77 | 0.77 | −0.80 | −0.02 | −1.19 | 0.38 | 0.35 | −0.39 |
mitochondrial-processing peptidase | 0.00 | −0.81 | 0.79 | −0.02 | 0.38 | 0.36 | −0.79 | −0.39 | −0.03 | −1.18 |
mitochondrial-processing peptidase | 0.22 | −0.92 | 0.75 | −0.40 | 0.69 | 0.29 | −0.53 | −0.47 | −0.18 | −1.22 |
ubiquitin carboxyl-terminal hydrolase | 0.66 | −0.50 | −0.17 | −1.32 | 0.68 | −0.65 | 0.83 | −0.02 | −0.66 | 0.15 |
guanine nucleotide-binding protein | 0.50 | −1.43 | 0.27 | −1.65 | 0.97 | −0.68 | 0.23 | −0.47 | −1.16 | −0.74 |
autophagy-related protein 3 | 1.01 | 0.32 | −0.21 | −0.90 | 1.34 | 0.44 | 1.22 | −0.33 | 0.11 | −0.12 |
COP9 signalosome complex subunit 5 | −0.52 | −0.53 | −1.26 | −1.28 | 0.40 | −0.87 | 0.74 | −0.92 | −1.80 | 0.34 |
Translation and related process | ||||||||||
40S ribosomal protein S20 | −1.57 | −1.73 | 0.00 | −0.17 | −0.69 | −0.86 | −1.56 | −0.88 | −1.74 | −0.88 |
60S ribosomal protein L9-like | −1.07 | −0.95 | 0.30 | 0.42 | −0.46 | −0.04 | −1.37 | −0.61 | −0.65 | −0.91 |
60S ribosomal protein L12 | −0.64 | −0.47 | 0.40 | 0.56 | −0.33 | 0.23 | −1.04 | −0.30 | −0.07 | −0.71 |
60S acidic ribosomal protein P0-like | 0.07 | −1.34 | 0.70 | −0.70 | 0.48 | −0.22 | −0.64 | −0.41 | −0.63 | −1.12 |
ribonuclease P protein subunit p25-like | −0.28 | −0.93 | −0.25 | −0.90 | 0.75 | −0.15 | −0.03 | −1.03 | −1.18 | −0.78 |
ribonucleoside-diphosphate reductase | 0.59 | −2.64 | 2.08 | −1.15 | 0.76 | −0.39 | −1.49 | −0.17 | −0.56 | −2.24 |
60S ribosomal protein L5 | 0.98 | −1.93 | 0.52 | −2.38 | 1.23 | −1.15 | 0.45 | −0.25 | −1.40 | −0.78 |
guanine nucleotide-binding protein | 1.01 | −1.33 | −0.13 | −2.46 | 1.78 | −0.68 | 1.13 | −0.77 | −1.46 | −0.65 |
ATP-dependent RNA helicase ddx6 | 2.86 | −0.74 | 0.15 | −3.44 | 1.48 | −1.96 | 2.70 | 1.37 | −0.58 | 1.22 |
Cytoskeleton and microtubule-based processes | ||||||||||
tubulin alpha-3 chain | −0.02 | −0.76 | 0.72 | −0.02 | 0.28 | 0.26 | −0.74 | −0.30 | −0.04 | −1.02 |
villin-2 | 1.25 | 0.41 | −0.57 | −1.41 | 1.08 | −0.33 | 1.82 | 0.17 | −0.15 | 0.74 |
dynein heavy chain | 1.50 | 0.39 | −0.28 | −1.38 | 1.66 | 0.28 | 1.77 | −0.16 | 0.12 | 0.12 |
clathrin light chain-like | 0.48 | −1.01 | −0.52 | −2.02 | 1.36 | −0.66 | 1.01 | −0.88 | −1.53 | −0.35 |
dynein intermediate chain 3, ciliary | 4.61 | −3.84 | 4.99 | −3.46 | 4.11 | 0.65 | −0.38 | 0.50 | 1.15 | −4.49 |
Unknown functions | ||||||||||
tartrate-resistant acid phosphatase ty. 5 | −2.28 | −1.51 | 1.19 | 1.95 | −2.80 | −0.85 | −3.47 | 0.52 | −0.33 | −0.66 |
hypothetical protein | −1.08 | 0.40 | −0.11 | 1.37 | −1.53 | −0.16 | −0.97 | 0.45 | 0.29 | 0.56 |
hypothetical protein | −1.62 | −0.57 | −0.03 | 1.02 | −1.51 | −0.49 | −1.59 | −0.11 | −0.60 | −0.08 |
hypothetical protein RFI_01644, partial | −0.32 | 0.62 | 0.13 | 1.07 | −0.91 | 0.16 | −0.45 | 0.59 | 0.75 | 0.46 |
hypothetical protein | −0.92 | 0.56 | −0.36 | 1.12 | −0.88 | 0.24 | −0.56 | −0.05 | 0.19 | 0.31 |
RING zinc finger-containing protein | 0.83 | −0.46 | −0.14 | −1.43 | 1.19 | −0.24 | 0.97 | −0.36 | −0.60 | −0.22 |
hypothetical protein RFI_36204, partial | −3.22 | −0.89 | −2.23 | 0.10 | 0.16 | 0.26 | −0.99 | −3.38 | −3.12 | −1.15 |
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Stuhr, M.; Cameron, L.P.; Blank-Landeshammer, B.; Reymond, C.E.; Doo, S.S.; Westphal, H.; Sickmann, A.; Ries, J.B. Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios. Oceans 2021, 2, 281-314. https://doi.org/10.3390/oceans2020017
Stuhr M, Cameron LP, Blank-Landeshammer B, Reymond CE, Doo SS, Westphal H, Sickmann A, Ries JB. Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios. Oceans. 2021; 2(2):281-314. https://doi.org/10.3390/oceans2020017
Chicago/Turabian StyleStuhr, Marleen, Louise P. Cameron, Bernhard Blank-Landeshammer, Claire E. Reymond, Steve S. Doo, Hildegard Westphal, Albert Sickmann, and Justin B. Ries. 2021. "Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios" Oceans 2, no. 2: 281-314. https://doi.org/10.3390/oceans2020017