Although reef-building corals are threatened by a number of anthropogenic impacts, certain scleractinian-dinoflagellate (genus Symbiodinium) endosymbioses have proven markedly resilient to environmental change. For instance, corals from upwelling habitats of Southern Taiwan withstand both short- and long-term increases in temperature, potentially due to their routine exposure to highly variable temperature regimes in situ. To gain a greater understanding of the proteomic basis for such acclimatization to unstable environmental conditions, specimens of the Indo-Pacific reef-building coral Seriatopora hystrix Dana 1846 were sampled during a period of stable temperature conditions from 1) a site characterized by frequent upwelling events in Southern Taiwan and 2) a nearby, non-upwelling control site in the Taiwan Strait. Two-dimensional gel electrophoresis followed by sequencing of differentially concentrated proteins with mass spectrometry unveiled significantly more proteins involved in the cellular stress response in coral hosts of the upwelling site. Although such stress protein signatures could be indicative of sub-lethal levels of cellular stress, especially given the relatively higher sediment loads characteristic of the upwelling site, these proteins may, in contrast, have been constitutively maintained at high levels in preparation for large fluctuations in temperature and other abiotic parameters ( e.g., nutrient levels) brought upon by upwelling events.
As Earth’s oceans continue to warm and acidify [
Southern Taiwan has served as an exemplary natural laboratory for understanding how environmental heterogeneity influences coral biology, as there are well-developed coral reefs experiencing very different oceanographic conditions in near vicinity of each other [
fluctuates more than a 1 - 2˚C within a single day. In contrast, the thermal environment of nearby (~15 km) Houbihu (HBH), which is just around the Maobitou Cape within Nanwan Bay (Taiwan’s southernmost embayment;
To gain greater insight into the molecular biology underlying the ability of corals to thrive in these upwelling environments, biopsies of the common, Indo-Pacific scleractinian Seriatopora hystrix Dana 1846 were taken from the same colonies from which laboratory-based experiments were previously conducted [
Both the upwelling site HBH (21˚56'18.01"N, 120˚44'45.54"E) and the non-upwelling site HWN (22˚01'23.30"N, 120˚41'18.29"E) have been well characterized with respect to their oceanography [
The temperature regimes of both the upwelling site HBH and the non-upwelling, Taiwan Strait, control site HWN (
As mentioned above, prior works on seriatoporid corals from HBH and HWN have focused mainly on these temperature differences as being responsible for the physiological heterogeneity documented across the sampled coral colonies (e.g., [
Sampling of six S. hystrix colonies (see insets of
Parameter | HBH | HWN | Type of test | Conclusion | Effect of husbandry | Ref(s) | |
---|---|---|---|---|---|---|---|
Seawater quality & ALCC (in situ data) | |||||||
Temperature (˚C)-monthly mean | 26.4 ± 1.8 | 26.6 ± 2.0 | student’s t-test | HBH = HWN | Not applicable (NA) | [ | |
Temperature (˚C)-monthly range | 6.3 ± 2.0 | 3.2 ± 0.6 | student’s t-test | HBH > HWN (2-fold) | NA | [ | |
Salinity | 32.7 ± 0.5 (SE) | 32.4 ± 0.23 (SE) | student’s t-test | HBH = HWN | Not significant (NS) | [ | |
Light at 7.5 m (PAR; μmol/m2/s) | 94 ± 9.1 | 94 ± 8.6 | student’s t-test | HBH = HWN | NS | [ | |
pH | 8.28 ± 0.03 (SE) | 8.29 ± 0.02 (SE) | student’s t-test | HBH = HWN | Not determined (ND) | [ | |
Dissolved oxygen (%) | 118 ± 3.0 (SE) | 126 ± 2.9 (SE) | student’s t-test | HBH = HWN | ND | [ | |
BOD5 (mg/L) | 1.1 ± 0.1 (SE) | 1.3 ± 0.1 (SE) | student’s t-test | HBH = HWN | ND | [ | |
[Nitrite] (μg/L) | 2.5 ± 0.5 (SE) | 7 ± 4 (SE) | student’s t-test | HBH = HWN | ND | [ | |
[Nitrate] (μg/L) | 49 ± 13 (SE) | 53 ± 9 (SE) | student’s t-test | HBH = HWN | ND | [ | |
[Ammonia] (μg/L) | 35 ± 11 (SE) | 63 ± 21 (SE) | student’s t-test | HBH = HWN | ND | [ | |
[Phosphate] (μg/L) | 3.5 ± 1.5 (SE) | 9 ± 3 (SE) | student’s t-test | HBH = HWN | ND | [ | |
[Silicate] (μg/L) | 600 ± 60 (SE) | 400 ± 80 (SE) | student’s t-test | HBH > HWN (1.5-fold) | ND | [ | |
[Suspended solids] (mg/L) | 20 ± 3 (SE) | 12 ± 2 (SE) | student’s t-test | HBH > HWN (1.6-fold) | ND | [ | |
Turbidity (NTU) | 7.2 ± 1.6 (SE) | 3.3 ± 0.8 (SE) | student’s t-test | HBH > HWN (2-fold) | ND | [ | |
[Chl-a] (μg/L) | 0.26 ± 0.07 (SE) | 0.25 ± 0.03 (SE) | student’s t-test | HBH = HWN | ND | [ | |
ALCC (%) | 43 ± 25 | 28 ± 25 | student’s t-test | HBH = HWN | ND | [ | |
Coral physiology and biological composition (in situ data for all response variables except growth, RNA/DNA ratio, protein/DNA ratio, and the Sym GCP) | |||||||
Growth (mg/cm2/day) | 0.8 ± 0.2 | 0.7 ± 0.2 | student’s t-test | HBH = HWN | ND (did not assess in situ) | [ | |
Sym density (cells/cm2) | 3.1 ± 1.0 | 3.0 ± 0.3 | Wilcoxon testa | HBH = HWN | Yes (increased), HWN > HBH post-exp. | [ | |
Areal chl-a (μg/cm2) | 2.8 ± 1.2 | 3.1 ± 0.8 | student’s t-testb | HBH = HWN | Yes (increased), HBH > HWN post-exp. | [ | |
Chl-a/cell (pg/cell) | 0.9 ± 0.3 | 1.0 ± 0.3 | student’s t-test | HBH = HWN | Yes (increased) | [ | |
Fv/Fm (dark-adapted) | 0.74 ± 0.01 | 0.75 ± 0.01 | student’s t-test | HBH = HWN | Yes (increased), HBH > HWN post-exp. | [ | |
RNA/DNA ratio | 0.4 ± 0.2 | 0.4 ± 0.1 | student’s t-testb | HBH = HWN | ND | [ | |
Parameter | HBH | HWN | Type of test | Conclusion | Effect of husbandry | Ref (s) |
---|---|---|---|---|---|---|
Protein/DNA ratio | 13 ± 4 | 18 ± 6 | student’s t-testb | HWN > HBH (1.4-fold) | ND | [ |
Sym GCP | 16 ± 7 | 15 ± 6 | student’s t-test | HBH = HWN | ND | [ |
Sym gene expression (normalized to the exogenous Solaris® RNA spike & Sym GCP as in Mayfield et al. [ | ||||||
Sym apx1 (stress response) | 2.8 ± 1.4 | 3.5 ± 2.5 | student’s t-test | HBH = HWN | ND | [ |
Sym hsp70 (stress response) | 670 ± 270 | 740 ± 290 | student’s t-testb | HBH = HWN | ND | [ |
Sym pgpase (photosynthesis) | 12 ± 5.2 | 13 ± 7.4 | student’s t-testc | HBH = HWN | ND | [ |
Sym psI (photosynthesis) | 101 ± 50 | 74 ± 51 | student’s t-testb | HBH > HWN (1.5-fold) | ND | [ |
Sym rbcL (photosynthesis) | 30 ± 21 | 40 ± 35 | student’s t-testc | HBH = HWN | ND | [ |
Sym nrt2 (metabolism) | 750 ± 230 | 1060 ± 760 | student’s t-testb | HBH = HWN | ND | [ |
Host coral gene expression (normalized to the exogenous Solaris® RNA spike & host GCP as in Putnam et al. [ | ||||||
Host hsp70 (stress response) | 75 ± 12 | 71 ± 11 | student’s t-test | HBH = HWN | ND | [ |
Host actb (cytoskeleton) | 110 ± 31 | 107 ± 33 | student’s t-testb | HBH = HWN | ND | [ |
Host ezrin (cytoskeleton) | 58 ± 35 | 80 ± 27 | student’s t-test | HBH = HWN | ND | [ |
Host trp1 (cytoskeleton) | 23 ± 8.2 | 28 ± 8.5 | student’s t-test | HBH = HWN | ND | [ |
Host tuba (cytoskeleton) | 230 ± 81 | 220 ± 51 | student’s t-test | HBH = HWN | ND | [ |
Host cplap2 (osmoregulation) | 1.5 ± 0.66 | 2.1 ± 0.78 | student’s t-test | HBH = HWN | ND | [ |
Host oatp (osmoregulation) | 5.7 ± 2.6 | 5.4 ± 1.6 | student’s t-test | HBH = HWN | ND | [ |
Host trcc (osmoregulation) | 210 ± 81 | 210 ± 76 | student’s t-testb | HBH = HWN | ND | [ |
Sym protein expression (western blot-derived; concentration normalized to the Sym GCP) | ||||||
Sym RBCL (photosynthesis) | 320 ± 170 | 200 ± 94 | student’s t-testb | HBH = HWN | ND | [ |
All 23 response variables listed above (standardized) | PERMANOVA | HBH = HWN | ND | herein | ||
Protein expression (2D + MS) | 15 proteins across 3 sequenced spots | 38 proteins across 6 sequenced spots | See text for details. | See text for details. | ND | Herein & [ |
aunequal variance; blog-transformed data; csquare root-transformed data.
data from the same coral colonies as those analyzed herein ( [
Proteins from one of the three technical replicates from each of three randomly chosen colonies from each of the two sites were purified as in Mayfield et al. [
Proteins (~130 μg) were electrophoresed across 2D as in Mayfield et al. [
In general, only protein spots that were uniquely synthesized by coral samples of one site and not the other in all three pairs of gels were removed from the final, representative gel and sequenced, though two protein spots that were instead more concentrated by HBH samples in all three gel pairs (i.e., DCPs, rather than USPs) were removed from the final HBH gel and analyzed by MS. In total three HBH > HWN and six HWN > HBH spots were in-gel digested with trypsin and purified as in Mayfield et al. [
When oceanographic (e.g., temperature), ecological (ALCC), and molecular physiological (i.e., the 23 response variables analyzed previously in the sampled colonies;
.MGF data files from the mass spectrometer (n = 6) were directly uploaded into the MS-SCAN program featured on the S. hystrix-Symbiodinium transcriptome server (http://symbiont.iis.sinica.edu.tw/s_hystrix/static/html/#mscan), and all default conditions of the MS-GF+ script [
When peptides could be identified with confidence (≥15 AA mapping to a translated contig in the S. hystrix-Symbiodinium transcriptome) with MS-SCAN, they were assigned a compartment of origin (host, Symbiodinium, intermediate [either host coral or Symbiodinium], or unknown), as well as a protein identity and functional category (e.g., metabolism) when the top hit contig (mRNA) hypothetically encoding the sequenced peptide aligned significantly (e < 10−5) to a functionally characterized protein in the NCBI nr database. The full mRNA sequence of the top hit contig derived from MS-SCAN analysis of the spectral data, rather than the peptide sequence itself, was used as the query (BLASTx) of the NCBI database; this is because trypsin-digested peptides are generally short (mean length = 22 ± 9 [std. dev.] AA herein; see
The compartmental breakdowns of the differentially concentrated proteomes were compared to the S. hystrix: Symbiodinium mRNA ratio of 1.8 [
As the transcriptomes of nubbins generated from the colonies analyzed herein were sequenced previously (6 nubbins from each site of origin sequenced after one month of experimental husbandry [
Although most seawater quality parameters were similar between HWN and HBH, several differed significantly upon pooling data over an eight-year period (
In addition to the 2D + MS results generated herein, we aimed to first provide a brief overview of previous findings obtained from these same coral colonies. We first summarize the influence of a one-month experimental husbandry on coral nubbins from the two study sites that were fragmented from the same source colonies from which biopsies were taken herein for 2D + MS analysis (“Effect of experimental husbandry”); these findings are described in detail in Mayfield et al. [
As discussed in more detail in Mayfield et al. [
Of the 23 response variables measured in corals of the two study sites (
Of the 6 and 3 protein spots concentrated at higher levels by samples of HWN (
With respect to the functional breakdown of all 49 proteins that could be assigned a compartment of origin (
align to characterized proteins, the dominant functional categories were cytoskeleton, stress response, transport, and transcription. Of the 14 HBH > HWN DCPs (
When looking only at the 29 host coral DCPs (
the most numerically dominant functional categories in the HWN > HBH differentially concentrated host coral proteome (
Spot (s) | Compartment | Contig | Identity | Functional category | Coverage (%) |
---|---|---|---|---|---|
1 | host | c71519_g1 | putative transcription factor Ovo-like 1 | transcription | 13 |
1 | host | c32821_g1 | leucine-rich repeat & IQ domain-containing protein 1 | unknown | 9 |
1 | host | c79274_g3 | von Willebrand factor D & EGF domain-containing protein | unknown | 8 |
1 | Sym | c146943_g1 | ubiquitin-40S ribosomal protein S27a | stress response | 35 |
1 | Sym | c30229_g1 | unknown | unknown | 25 |
1 | Sym | c288_g1 | adenylate cyclase | metabolism | 6 |
2 | host | c73482_g1 | unknown | unknown | 16 |
2 | host | c63186_g1 | unknown | unknown | 12 |
2 | host | c69424_g1* | unknown | unknown | 12 |
2,5 | host | c79716_g1 | debrin-like | cell migration/ actin binding | 8 |
3 | host | c86107_g1a | unknown | unknown | 19 |
3-5 | host | c65959_g1 | Rho GDP-dissociation inhibitor 1 | cytoskeleton | 16 |
3 | host | c69652_g1 | unknown | unknown | 8 |
3 | host | c76783_g1a | serine/arginine repetitive matrix protein 2 | RNA processing | 7 |
3 | host | c80461_g1 | voltage-dependent R-type calcium channel subunit alpha-1E-like isoform X2 | transport | 1 |
3 | Sym | c75440_g1b | fucoxanthin-chlorophyll a-c binding protein | photosynthesis | 24 |
3 | Sym | c28876_g1 | unknown | unknown | 17 |
3 | Sym | c192890_g1 | bestrophin/alpha-ketoglutarate-dependent dioxygenase alkB-like | transport | 16 |
3 | Sym | c147855_g1 | hippocalcin-like protein 1 | transport | 13 |
3 | Sym | c117310_g1 | alpha-1,2-mannosyltransferase ALG9 | metabolism | 6 |
4 | host | c62634_g1 | protamine | DNA stabilization | 14 |
4 | host | c80550_g3 | Prolow-density lipoprotein receptor-related protein 1 | endocytosis | 3 |
5 | host | c167493_g1 | unknown | unknown | 63 |
5 | host | c168524_g1 | short-chain collagen C4 | structural | 22 |
5 | host | c170150_g1 | unknown | unknown | 16 |
5 | host | c77868_g2a | eukaryotic translation initiation factor 3 subunit A-like | translation | 12 |
5 | host | c72431_g1 | Schlafen family member 5 | cell differentiation | 3 |
5 | Sym | c51777_g1 | unknown | unknown | 14 |
5 | Sym | c97047_g1 | unknown | unknown | 10 |
5 | Sym | c13654_g1* | ankyrin repeat domain-containing protein 50 | unknown | 4 |
Spot (s) | Compartment | Contig | Identity | Functional category | Coverage (%) |
---|---|---|---|---|---|
5 | Sym | c52097_g1 | DEAD-box ATP-dependent RNA helicase 35 | RNA processing | 3 |
5 | unknown | c46638_g1 | unknown | unknown | 51 |
5 | unknown | c45226_g1 | unknown | unknown | 33 |
5 | unknown | c41865_g1* | unknown | unknown | 18 |
6 | host | c52240_g1 | unknown | unknown | 14 |
6 | Sym | c29807_g1 | serine/threonine protein kinase pelle | signal transduction | 3 |
6 | Sym | c37817_g1 | unknown | unknown | 3 |
6 | Sym | c48738_g1 | DNA topoisomerase I | DNA replication | 3 |
aMaintained at lower concentrations in corals exposed to variable temperature regimes [
Spot | Compartment | Contig | Identity | Functional category | Coverage (%) |
---|---|---|---|---|---|
1 (DCP) | host | c69816_g1 | actin | cytoskeleton | 27 |
1 | host | c41229_g1 | unknown | unknown | 22 |
1 | host | c58883_g1* | O-aminophenol oxidase | stress response | 11 |
1 | host | c80336_g3 | RIMS-binding protein | neurotransmission | 9 |
1 | host | c76524_g1 | RNA polymerase-associated protein CTR9-like | RNA processing/editing | 4 |
1 | intermediate | c36639_g1 | RNA recognition motif (RRM) superfamily | RNA processing/editing | 8 |
2 (DCP) | host | c64389_g2 | gelsolin-like | cytoskeleton | 27 |
2 | host | c59669_g2 | unknown | unknown | 10 |
2 | Sym | c103934_g1 | unknown | unknown | 15 |
2 | Sym | c185341_g1 | unknown | unknown | 13 |
2 | Sym | c61072_g1 | HSPB1-associated protein 1-like | stress response | 10 |
3 (USP) | host | c62707_g1a | beta-gamma crystallin | stress response | 34 |
3 | host | c108872_g1 | protein split ends isoform X1 | transcriptional repression | 12 |
3 | Sym | c31796_g1 | unknown | unknown | 21 |
3 | Sym | c37656_g1 | unknown | unknown | 4 |
aMaintained at lower concentrations in corals exposed to variable temperature regimes [
In general, the same functional categories differed in proportional abundance between sites of origin for Symbiodinium (
Only five Symbiodinium proteins were identified across the three HBH > HWN protein spots, and only one could be identified with confidence (
The congruency between mRNA and protein expression did not differ between the two compartments of the S. hystrix-Symbiodinium endosymbiosis (2-sample proportion tests, P > 0.05). Specifically, 2 of the 29 host coral molecules (7%) and 1 of the 20 Symbiodinium molecules (5%) demonstrated congruency between mRNA expression and protein concentration. These three molecules included 1) a host O-aminophenol oxidase involved in the oxidative stress response (the lone HBH > HWN molecule demonstrating congruency between mRNA and protein expression; 7%;
Besides a host coral beta-gamma crystallin protein, only three additional proteins were found to be differentially concentrated between sites of origin herein and between stable and variable temperature treatments in S. hystrix nubbins made from these same colonies by Mayfield et al. [
Cell and molecular biology-driven approaches have aided in developing our understanding of both the fundamental biology of anthozoan-dinoflagellate endosymbioses [
If diminished UVR levels were reaching the HBH S. hystrix colonies, then they could be hypothesized to be at lower risk of high temperature + UVR-induced bleaching [
Given the fact that mean monthly temperature range, silicate concentrations, and suspended solid levels and turbidity were all higher at HBH (the upwelling site), it is tempting to speculate that the relatively higher number of stress response-associated proteins within the HBH > HWN proteome is indicative of sub-lethal levels of cellular stress in corals of HBH. However, the physiological performance of these corals did not differ from those of HWN ( [
Osmoregulation has been hypothesized to be the crux of the coral stress and bleaching response [
Unfortunately, it has become commonplace in the coral biology field to make conjectures about protein behavior based on mRNA expression data alone (sensu [
The authors would like to thank Dr. Yu-Bin Wang for developing the MS-SCAN software and implementing it on the S. hystrix-Symbiodinium transcriptome server, as well as Drs. Peter Edmunds and Tung-Yung Fan for fruitful discussions on the eco-physiology of corals of Southern Taiwan. This work was funded by the United States National Science Foundation (postdoctoral research fellowship to ABM; OISE-0852960) and the Khaled bin Sultan Living Oceans Foundation (postdoctoral research fellowship to ABM).
Mayfield, A.B., Chen, Y.-J., Lu, C.-Y. and Chen, C.-S. (2018) Exploring the Environmental Physiology of the Indo-Pacific Reef Coral Seriatopora hystrix with Differential Proteomics. Open Journal of Marine Science, 8, 223-252. https://doi.org/10.4236/ojms.2018.82012
Name | Length (#AA) | Sequence | Protein identity |
---|---|---|---|
HBH > HWN spot 1, protein 1 (c41229_g1) | 39 | AIYEMKKKLGVNIKFIHVVRNPFDNIATMVLQHKAIKGR* | unknown host |
HBH > HWN spot 1, protein 2 (c58883_g1) | 30 | QLRRLGVKKKERRHARKLLKKELEPKKRIR* | host O-aminophenol oxidase |
HBH > HWN spot 1, protein 3, peptide 1 (c69816_g1) | 21 | AGFAGDDAPRAVFPSIVGRPR* | host actin |
HBH > HWN spot 1, protein 3, peptide 2 (c69816_g1) | 12 | DSYVGDEAQSKR | |
HBH > HWN spot 1, protein 3, peptide 3 (c69816_g1) | 29 | IWHHTFYNELRVAPEEHPVLLTEAPLNPK* | |
HBH > HWN spot 1, protein 3, peptide 4 (c69816_g1) | 10 | GYSFTTTAER | |
HBH > HWN spot 1, protein 3, peptide 5 (c69816_g1) | 16 | SYELPDGQVITIGNER | |
HBH > HWN spot 1, protein 3, peptide 6 (c69816_g1) | 13 | QEYDESGPSIVHR | |
HBH > HWN spot 1, protein 4, peptide 1 (c80336_g3) | 18 | QRAKDLAEHAKALLSKEK | host RIMS-binding protein |
HBH > HWN spot 1, protein 4, peptide 2 (c80336_g3) | 19 | LEVSDVKCGLLTDECNKLK | |
HBH > HWN spot 1, protein 5, peptide 1 (c36639_g1) | 22 | GHQHWDNNYWRKDDRRPSRYWR | RNA recognition motif superfamilya |
HBH > HWN spot 1, protein 5, peptide 2 (c36639_g1) | 24 | QKRRRRRKMDETGQPQRHLKRRKR | |
HBH > HWN spot 1, protein 6, peptide 1 (c76524_g1) | 32 | FFKHHNVEVLLYLARAYFKAGKLKECKQILLK | host RNA polymerase-associated protein CTR9-like |
HBH > HWN spot 1, protein 6, peptide 2 (c76524_g1) | 29 | TFVKKVPKTDKSDPKRLKKDLPKILKTLK | |
HBH > HWN spot 2, protein 1, peptide 1 (c64389_g2) | 13 | DSNLALFGSDLEK | host gelsolin-like |
HBH > HWN spot 2, protein 1, peptide 2 (c64389_g2) | 14 | FYNGDSYIILNTYK |
Name | Length (#AA) | Sequence | Protein identity |
---|---|---|---|
HBH > HWN spot 2, protein 1, peptide 3 (c64389_g2) | 28 | ESTQDEYGTAAYKTVELDTLNDKPVQHR* | |
HBH > HWN spot 2, protein 1, peptide 4 (c64389_g2) | 18 | KYFSQLELLTGGADSGFR | |
HBH > HWN spot 2, protein 1, peptide 5 (c64389_g2) | 38 | VTEVAYCKESITPDNVYVIDNGEEIYQINGSSSDKDER* | |
HBH > HWN spot 2, protein 1, peptide 6 (c64389_g2) | 9 | AAQYCQSLK | |
HBH > HWN spot 2, protein 1, peptide 7 (c64389_g2) | 46 | EGGFGGLPSGDPDTEDPIDDDFEPTIKKISDASGHLELSDTSGFSK* | |
HBH > HWN spot 2, protein 1, peptide 8 (c64389_g2) | 9 | DVFIVDNGK | |
HBH > HWN spot 2, protein 1, peptide 9 (c64389_g2) | 10 | HPLVPVSVVK | |
HBH > HWN spot 2, protein 2 (c103934_g1) | 39 | LEKLEKLARKAAEKMQKKKDKKGKKDKKKDKKSKKDKKK* | unknown Sym |
HBH > HWN spot 2, protein 3 (c185341_g1) | 39 | DDRDRDRGHDRERSFEERRPRDDRDGRYRDDRDGRDRGR* | unknown Sym |
HBH > HWN spot 2, protein 4 (c61072_g1) | 46 | VRQVPSGLTQPCTLVPKRGHEPVWRHWNISFWKEACGLEYCNCRSR* | Sym HSPB1-associated protein 1-like |
HBH > HWN spot 2, protein 5, peptide 1 (c59669_g2) | 19 | DEEDEEASKEDEEKEDEAK | unknown host |
HBH > HWN spot 2, protein 5, peptide 2 (c59669_g2) | 19 | CQWPCMWPCCCECDPPKFK | |
HBH > HWN spot 3, protein 1, peptide 1 (c31796_g1) | 35 | ADTAASESEGAKYDEPDTETEDEADKHRRLPMHGR | unknown Sym |
HBH > HWN spot 3, protein 1, peptide 2 (c31796_g1) | 28 | SKVKAKAKAKAKAKAKAKPKAKAKAKAK | |
HBH > HWN spot 3, protein 2, peptide 1 (c108872_g1) | 18 | THRERQRQDEELREQKER | host protein split ends isoform X1 |
HBH > HWN spot 3, protein 2, peptide 2 (c108872_g1) | 22 | EKERKEKEQREREAREREQRER | |
HBH > HWN spot 3, protein 3, peptide 1 (c62707_g1) | 16 | NGLGEEFTGSDANLKK | host beta-gamma crystallin |
HBH > HWN spot 3, protein 3, peptide 2 (c62707_g1) | 9 | HGFYGGFSK | |
HBH > HWN spot 3, protein 3, peptide 3 (c62707_g1) | 35 | GAGVSSAIVLSKNENFAIFTETNYKGIE QQLDAGK** |
Name | Length (#AA) | Sequence | Protein identity |
---|---|---|---|
HBH > HWN spot 3, protein 4 (c37656_g1) | 18 | DRSKAALDTKAEPKDRSK | unknown Sym |
HWN > HBH spot 1, protein 1 (c146943_g1) | 26 | KKTYTKPKKIKHKRKKVKLAVLKFYK* | Sym ubiquitin-40S ribosomal protein S27a |
HWN > HBH spot 1, protein 2 (c30229_g1) | 31 | KKEKAVKKKDKKKDKKDKKKKKD KKGKKKKK** | unknown Sym |
HWN > HBH spot 1, protein 3, peptide 1 (c71519_g1) | 18 | KTFRPKLTSENQMECFKK | host putative transcription factor Ovo-like 1 |
HWN > HBH spot 1, protein 3, peptide 2 (c71519_g1) | 32 | DNQSEFMTHMANVHPDREKGPW MNKNTNLCAR | |
HWN > HBH spot 1, protein 4, peptide 1 (c32821_g1) | 33 | TRKEFQPLLEAKKLERVKKRNEELDRIERVERK | host leucine-rich repeat and IQ domain-containing protein 1 |
HWN > HBH spot 1, protein 4, peptide 2 (c32821_g1) | 15 | KKEEEKRTREEIQRK | |
HWN > HBH spot 1, protein 5, peptide 1 (c79274_g3) | 21 | CECYENYHSPETGCDRSFCAK | host von Willebrand factor D and EGF domain-containing protein |
HWN > HBH spot 1, protein 5, peptide 2 (c79274_g3) | 26 | KCHCDEGWDNQIHVSGFNAHFGPCKK | |
HWN > HBH spot 1, protein 6, peptide 1 (c288_g1) | 25 | AARMSRVGTKAGRVVRLLRLVRLIR | Sym adenylate cyclase |
HWN > HBH spot 1, protein 6, peptide 2 (c288_g1) | 32 | RGQQRDPDAESDAKRNCCSRCCSATLKCIRRR | |
HWN > HBH spot 2, protein 1 (c63186_g1) | 29 | KTVKMIEKQLALKKLKKKSKISKKHPKKK* | unknown host |
HWN > HBH spot 2, protein 2, peptide 1 (c69424_g1) | 20 | DIDYGCMEGSCAMEYCQHTK | unknown host |
HWN > HBH spot 2, protein 2, peptide 2 (c69424_g1) | 26 | CGQKEDCRKAAESWGNCKAFSCFANR | |
HWN > HBH spot 2, protein 3, peptide 1 (c73482_g1) | 20 | CRNWSQCKKDECCIRYSVNK | unknown host |
HWN > HBH spot 2, protein 3, peptide 2 (c73482_g1) | 15 | TTKWGQKKHRCERLR | |
HWN > HBH spot 2, protein 4 (c79716_g1) | 41 | RLADERKMLEEEEMQRQIDMERRRKEEEERRKRDTEERRKR* | host debrin-like |
HWN > HBH spot 3, protein 1 (c117310_g1) | 36 | EERKRQRHEAIWKEWKKLLRSLVVYVKFRLPLRKTR* | Sym alpha-1,2-mannosyltransferase ALG9 |
Name | Length (#AA) | Sequence | Protein identity |
---|---|---|---|
HWN > HBH spot 3, protein 2, peptide 1 (c147855_g1) | 21 | EHPLILAWQALFNGYWNTKSR | Sym hippocalcin-like protein 1 |
HWN > HBH spot 3, protein 2, peptide 2 (c147855_g1) | 15 | WRGKTDNSWLEYVKK | |
HWN > HBH spot 3, protein 3, peptide 1 (c192890_g1) | 22 | MSLLQHWRCSLRSHVRFLRTSR | Sym bestrophin/ alpha-ketoglutarate-dependent dioxygenase AlkB-like |
HWN > HBH spot 3, protein 3, peptide 2 (c192890_g1) | 38 | INCCFDAIFTTVHRGQMLGVYSSEL ASGMYELASNMFR | |
HWN > HBH spot 3, protein 4, peptide 1 (c28876_g1) | 16 | DRSRSPHRSPRRSPRR | unknown Sym |
HWN > HBH spot 3, protein 4, peptide 2 (c28876_g1) | 22 | DDRWKDRNDRNDRSDRSDRNDR | |
HWN > HBH spot 3, protein 5, peptide 1 (c65959_g1) | 17 | TLDEIQKLDAEDESLVR** | host Rho GDP-dissociation inhibitor 1 |
HWN > HBH spot 3, protein 5, peptide 2 (c65959_g1) | 15 | AGPQEYLTPLDEAPK | |
HWN > HBH spot 3, protein 6, peptide 1 (c69652_g1) | 38 | KENKSKPNHAAKSKVAKKKKLKVKGTPLTSLSKTVTYK | unknown host |
HWN > HBH spot 3, protein 6, peptide 2 (c69652_g1) | 25 | HCHASCLTNCLPSCGSGCCSADEER | |
HWN > HBH spot 3, protein 7, peptide 1 (c75440_g1) | 28 | DSTETGEPGNYGVGFPTFLGKVEDPEAR** | Sym fucoxanthin-chlorophyll a-c binding protein |
HWN > HBH spot 3, protein 7, peptide 2 (c75440_g1) | 8 | LAAELANGR | |
HWN > HBH spot 3, protein 7, peptide 3 (c75440_g1) | 26 | ELGVQDPIGFWDPLGLSADKDEATFK | |
HWN > HBH spot 3, protein 8, peptide 1 (c76783_g1) | 31 | TPVSESSDERSNSDSSDHNLERESSPVKRRK | host serine/arginine repetitive matrix protein 2 |
HWN > HBH spot 3, protein 8, peptide 2 (c76783_g1) | 32 | QRHLDKSDARRERKMRDDHENRHDEERLRRER | |
HWN > HBH spot 3, protein 9 (c80461_g1) | 25 | KTVKVLRVLRVLRPLKAINKAKKLK* | host voltage-dependent R-type calcium channel subunit alpha-1E-like isoform X2 |
HWN > HBH spot 3, protein 10, peptide 1 (c86107_g1) | 20 | TRKLKSRIIKRIRRLRVLRR | unknown host |
HWN > HBH spot 3, protein 10, peptide 2 (c86107_g1) | 21 | KAKQVLVKRVRKMKRKIKRRK |
Name | Length (#AA) | Sequence | Protein identity |
---|---|---|---|
HWN > HBH spot 4, protein 1 (c62634_g1) | 28 | SVKKVTKKAKKAKKAKKVIRKRKAPAKR* | host protamine |
HWN > HBH spot 4, protein 2, peptide 1 (c80550_g3) | 14 | FTCANGHCINFDWK | host prolow-density lipoprotein receptor-related protein 1 |
HWN > HBH spot 4, protein 2, peptide 2 (c80550_g3) | 20 | RWQCDGEDDCGDGSDEGLCK | |
HWN > HBH spot 4, protein 2, peptide 3 (c80550_g3) | 29 | CVMMSYVCDGYNDCGDASDEHPKEGCLLR | |
HWN > HBH spot 5, protein 1, peptide 1 (c13654_g1) | 22 | EYMEQWDQATIAFRTGYEVAKR | Sym ankyrin repeat domain-containing protein 50 |
HWN > HBH spot 5, protein 1, peptide 2 (c13654_g1) | 16 | VILIQAAARGFLIRRR | |
HWN > HBH spot 5, protein 2 (c167493_g1) | 60 | LTVQVVVRTQEGSYIGETRYTYNSNLLSQFEQCVKAMDDEDMELDCTGSP* | unknown host |
HWN > HBH spot 5, protein 3 (c168524_g1) | 27 | TLLLRKRKSLTLSLESLGKRLKVLELR* | host short-chain collagen C4 |
HWN > HBH spot 5, protein 4 (c170150_g1) | 34 | KSTKVMHNFEDDDGNNEEED KENDSGFGRYEEMR* | unknown host |
HWN > HBH spot 5, protein 5, peptide 1 (c41865_g1) | 30 | NLRFPHLLRFPDLPHLLKRKLRQQRKRPLR | unknown |
HWN > HBH spot 5, protein 5, peptide 2 (c41865_g1) | 32 | HRQLRVRQTQQLRLQGLLPLLSQLRRRNQRHR | |
HWN > HBH spot 5, protein 6 (c45226_g1) | 31 | DDDGDKWLDNESNDFSSSEGEVDDNEKDDWK* | unknown |
HWN > HBH spot 5, protein 7 (c46638_g1) | 29 | KGSKKKKGSKKKKGSKKKKKKGKKKGKKK* | unknown |
HWN > HBH spot 5, protein 8, peptide 1 (c51777_g1) | 18 | TQMIPNRTYCIWYQVEPR | unknown Sym |
HWN > HBH spot 5, protein 8, peptide 2 (c51777_g1) | 38 | DQPLETKPLETVRLAQLLSLGFT VISEEANSLDSELYK | |
HWN > HBH spot 5, protein 9 (c52097_g1) | 30 | LRKKIREATLAGIREKKKHVDRMHRKRRFR* | Sym DEAD-box ATP-dependent RNA helicase 35 |
HWN > HBH spot 5, protein 10 (c72431_g1) | 30 | KPKKEKKKKKGKKEKKKKDKKDKKEKKKKK* | host Schlafen family member 5 |
HWN > HBH spot 5, protein 11, peptide 1 (c77868_g2) | 36 | KRLEERRRERILERKVQRRIEREE KERKEKEEREKR | host eukaryotic translation initiation factor 3 subunit A-like |
HWN > HBH spot 5, protein 11, peptide 2 (c77868_g2) | 20 | WRDDRGRDDRGRDDRWRVDR |
Name | Length (#AA) | Sequence | Protein identity |
---|---|---|---|
HWN > HBH spot 5, protein 12 (c97047_g1) | 24 | KKDKKKSDKKKKKDKKKKKDKKKK** | unknown Sym |
HWN > HBH spot 6, protein 1 (c29807_g1) | 18 | YLRILRLLRLARLLRVIK | Sym serine/threonine protein kinase pelle |
HWN > HBH spot 6, protein 2 (c37817_g1) | 21 | VTEVVLLEREQRVRARLLRPK | unknown Sym |
HWN > HBH spot 6, protein 3 (c48738_g1) | 20 | EKKHKDKEHKKDKKEKKEKK | Sym DNA topoisomerase I |
HWN > HBH spot 6, protein 4 (c52240_g1) | 28 | RFKGILKIRRKKMKKHKYRKRRKRDLFK* | unknown host |
mean length of sequenced peptide (excluding overlapping samples) | 22 ± 9 (std. dev.) AA | ||
total number of proteins | 53 | ||
total number of contiguous peptide sequences | 95 | ||
total number of peptides sequenced | 129 |
acompartment of origin could not be verified.