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Oellermann, Michael; Strugnell, Jan M; Lieb, Bernhard; Mark, Felix Christopher (2015): DNA alignment and Bayesian trees of partial sequences of COI, COIII and the haemocyanin functional unit f-g of 28 octopod species [dataset]. PANGAEA, https://doi.org/10.1594/PANGAEA.839802, Supplement to: Oellermann, M et al. (2015): Positive selection in octopus haemocyanin indicates functional links to temperature adaptation. BMC Evolutionary Biology, 15, 133-150, https://doi.org/10.1186/s12862-015-0411-4

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Abstract:
Background: Octopods have successfully colonised the world's oceans from the tropics to the poles. Yet, successful persistence in these habitats has required adaptations of their advanced physiological apparatus to compensate impaired oxygen supply. Their oxygen transporter haemocyanin plays a major role in cold tolerance and accordingly has undergone functional modifications to sustain oxygen release at sub-zero temperatures. However, it remains unknown how molecular properties evolved to explain the observed functional adaptations. We thus aimed to assess whether natural selection affected molecular and structural properties of haemocyanin that explains temperature adaptation in octopods.
Results: Analysis of 239 partial sequences of the haemocyanin functional units (FU) f and g of 28 octopod species of polar, temperate, subtropical and tropical origin revealed natural selection was acting primarily on charge properties of surface residues. Polar octopods contained haemocyanins with higher net surface charge due to decreased glutamic acid content and higher numbers of basic amino acids. Within the analysed partial sequences, positive selection was present at site 2545, positioned between the active copper binding centre and the FU g surface. At this site, methionine was the dominant amino acid in polar octopods and leucine was dominant in tropical octopods. Sites directly involved in oxygen binding or quaternary interactions were highly conserved within the analysed sequence.
Conclusions: This study has provided the first insight into molecular and structural mechanisms that have enabled octopods to sustain oxygen supply from polar to tropical conditions. Our findings imply modulation of oxygen binding via charge-charge interaction at the protein surface, which stabilize quaternary interactions among functional units to reduce detrimental effects of high pH on venous oxygen release. Of the observed partial haemocyanin sequence, residue 2545 formed a close link between the FU g surface and the active centre, suggesting a role as allosteric binding site. The prevalence of methionine at this site in polar octopods, implies regulation of oxygen affinity via increased sensitivity to allosteric metal binding. High sequence conservation of sites directly involved in oxygen binding indicates that functional modifications of octopod haemocyanin rather occur via more subtle mechanisms, as observed in this study.
Related to:
Aguado Giménez, F; García García, B (2002): Growth and food intake models in Octopus vulgaris Cuvier (1797): influence of body weight, temperature, sex and diet. Aquaculture International, 10(5), 361-377, https://doi.org/10.1023/A:1023335024053
Artegiani, Antonio; Paschini, Elio; Russo, Antonio; Bregant, Davide; Raicich, Fabio; Pinardi, Nadia (1997): The Adriatic Sea General Circulation. Part I: Air–Sea Interactions and Water Mass Structure. Journal of Physical Oceanography, 27(8), 1492-1514, https://doi.org/10.1175/1520-0485(1997)027%3C1492:TASGCP%3E2.0.CO;2
Barnes, David K A; Fuentes, Veronica; Clarke, Andrew; Schloss, Irene R; Wallace, Margaret I (2006): Spatial and temporal variation in shallow seawater temperatures around Antarctica. Deep Sea Research Part II: Topical Studies in Oceanography, 53(8-10), 853-865, https://doi.org/10.1016/j.dsr2.2006.03.008
Boyle, P R (1981): Methods for the aquarium maintenance of the common octopus of British waters, Eledone cirrhosa. Laboratory Animals, 15(4), 327-331, https://doi.org/10.1258/002367781780952807
Burdick, David; Brown, Valerie; Asher, Jacob; Gawel, Mike; Goldman, Lee; Hall, Amy; Kenyon, Jean; Leberer, Trina; Lundblad, Emily; McIlwain, Jenny; Miller, Joyce; Minton, Dwayne; Nadon, Marc; Pioppi, Nick; Raymundo, Laurie; Richards, Benjamin; Schroeder, Robert; Schupp, Peter; Smith, Ellen; Zgliczynski, Brian (2008): The state of coral reef ecosystems of Guam. In: Waddell, Jenny; Clarke, Alicia (eds.) The State of Coral Reef Ecosystems of the United States and Pacific Freely Associated States: 2008, 465-509
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Furevik, Tore (2001): Annual and interannual variability of Atlantic Water temperatures in the Norwegian and Barents Seas: 1980–1996. Deep Sea Research Part I: Oceanographic Research Papers, 48(2), 383-404, https://doi.org/10.1016/S0967-0637(00)00050-9
Mangold, K; von Boletsky, Sigurd; Frösch, D (1971): Reproductive biology and embryonic development of Eledone cirrosa (Cephalopoda: Octopoda). Marine Biology, 8(2), 109-117, https://doi.org/10.1007/BF00350926
Miliou, Helen; Fintikaki, Myrsini; Kountouris, Triantaphyllos; Verriopoulos, George (2005): Combined effects of temperature and body weight on growth and protein utilization of the common octopus, Octopus vulgaris. Aquaculture, 249(1-4), 245-256, https://doi.org/10.1016/j.aquaculture.2005.03.038
Muus, Bent (2002): The Bathypolypus-Benthoctopus problem of the North Atlantic. Malacologia, 44(2), 175-222, http://bionames.org/references/aab31dc1f1ee9342ee9495d667845a6d
Nabhitabhata, Jaruwat (2014): Amphioctopus aegina. In: José Iglesias, Lidia Fuentes, Roger Villanueva (eds.) Cephalopod Culture. Springer, 349-363, https://doi.org/10.1007/978-94-017-8648-5_18
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Promboon, Pichitra; Nabhitabhata, Jaruwat; Duengdee, Teerapong (2011): Life cycle of the marbled octopus, Amphioctopus aegina (Gray) (Cephalopoda:Octopodidae) reared in the laboratory. Scientia Marina, 75(4), 811-821, https://doi.org/10.3989/scimar.2011.75n4811
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Coverage:
Median Latitude: -19.904138 * Median Longitude: -7.694828 * South-bound Latitude: -70.510000 * West-bound Longitude: -124.430000 * North-bound Latitude: 79.620000 * East-bound Longitude: 169.630000
Parameter(s):
Size:
603 data points

Data

Download dataset as tab-delimited text — use the following character encoding:


ID
(Animal identifier)

Species

Expedition

Station

Gear
(Fishing gear)

Sampling date
(Date of capture)

Latitude

Longitude

Bathy depth [m]
10 
Location
11 
Temp [°C]
(at depth)
12 
Temp min [°C]
13 
Temp max [°C]
14 
Reference
(Temperature)
15 
Sal
(PSU, at depth)
16 
Sal min
17 
Sal max
18 
Reference
(Salinity)
19 
Samp m [g]
(Total weight)
20 
Samp m [g]
(Gutted weight)
21 
l [mm]
(Mantle length)
22 
Sex
23 
Comment
O85Adelieledone polymorphaANT-XXVII/3PS77/260-6Agassiz Trawl2011-03-20-70.51-10.36253Antarctic Ocean, Eastern Weddel Sea-1.034.583.3061.0female
O187Amphioctopus aeginaIndian Ocean28.030.0Promboon et al. (2011); Nabhitabhata (2014); Phanichpong (1985)30.0Promboon et al. (2011)Position not given
O32Amphioctopus aegina5.4889.47Indian Ocean28.030.0Promboon et al. (2011); Nabhitabhata (2014); Phanichpong (1985)30.0Promboon et al. (2011)Asia market, approximate location
O143Bathypolypus arcticus21232007-09-2479.1326.10256Barents Sea4.011.0Wood et al. (1998); O'Dor and Macalaster (1983); Muus (2002)
O144Bathypolypus arcticus20222007-09-1278.9711.57315Barents Sea4.011.0Wood et al. (1998); O'Dor and Macalaster (1983); Muus (2002)
O133Bathypolypus pugniger20352003-09-1279.628.00688Barents Sea0.03.0Muus (2002); Furevik (2001)34.935.1Muus (2002); Furevik (2001)
O134Bathypolypus pugniger20352007-09-1379.628.00688Barents Sea0.03.0Muus (2002); Furevik (2001)34.935.1Muus (2002); Furevik (2001)
O135Bathypolypus pugniger20352007-09-1379.628.00688Barents Sea0.03.0Muus (2002); Furevik (2001)34.935.1Muus (2002); Furevik (2001)
O136Bathypolypus pugniger23342007-08-0873.1718.07443Barents Sea0.03.0Muus (2002); Furevik (2001)34.935.1Muus (2002); Furevik (2001)
O145Bathypolypus pugniger26662007-08-1771.2728.62409Barents Sea0.03.0Muus (2002); Furevik (2001)34.935.1Muus (2002); Furevik (2001)
O39Benthoctopus cf. longibrachusANT-XXVII/3PS77/208-5Agassiz Trawl2011-02-11-54.32-56.10292Antarctic Ocean, Burdwood Bank4.934.15.1024.0
O52Benthoctopus cf. longibrachusANT-XXVII/3PS77/211-5Agassiz Trawl2011-02-14-53.24-42.41320Antarctic Ocean, Shag Rocks2.134.427.0
O41Benthoctopus cf. rigbyaeANT-XXVII/3PS77/208-5Agassiz Trawl2011-02-11-54.32-56.10292Antarctic Ocean, Burdwood Bank4.934.1
O44Benthoctopus cf. rigbyaeANT-XXVII/3PS77/208-5Agassiz Trawl2011-02-11-54.32-56.10292Antarctic Ocean, Burdwood Bank4.934.1
O45Benthoctopus cf. rigbyaeANT-XXVII/3PS77/208-5Agassiz Trawl2011-02-11-54.32-56.10292Antarctic Ocean, Burdwood Bank4.934.1
O48Benthoctopus cf. rigbyaeANT-XXVII/3PS77/208-5Agassiz Trawl2011-02-11-54.32-56.10292Antarctic Ocean, Burdwood Bank4.934.1
O49Benthoctopus cf. rigbyaeANT-XXVII/3PS77/208-5Agassiz Trawl2011-02-11-54.32-56.10292Antarctic Ocean, Burdwood Bank4.934.1
O82Benthoctopus sp.ANT-XXVII/3PS77/208-3Bottom Trawl2011-02-11-54.32-56.90286Antarctic Ocean, Burdwood Bank4.934.111.3021.0male
O148Callistoctopus macropusSummer 201035.1333.43Mediterranean Sea, Cyprus16.822.8Fuentès and Offner (2001)
O180Callistoctopus ornatus-18.20146.90Pacific Ocean, Eastern Australia25.030.0Fields et al. (1976); Burdick et al. (2008)approximate location
O186Eledone cirrhosa58.90-0.29North Atlantic Ocean13.016.0Mangold et al. (1971); Boyle (1981)approximate location
O147Eledone moschataSummer 201035.1333.43Mediterranean Sea, Cyprus10.021.0Artegiani et al. (1997)460.2
O150Eledone moschata200845.2212.28Mediterranean Sea, Italy, Chioggia,10.021.0Artegiani et al. (1997)35.0male
O151Eledone moschata200845.2212.28Mediterranean Sea, Italy, Chioggia,10.021.0Artegiani et al. (1997)35.0
O152Eledone moschata200845.2212.28Mediterranean Sea, Italy, Chioggia,10.021.0Artegiani et al. (1997)35.0
EdofEnteroctopus dofleini44.60-124.43Pacific Ocean, Oregon USA3.013.0Rigby and Sakurai (2004)
O36Graneledone yamanaANT-XXVII/3PS77/208-5Agassiz Trawl2011-02-11-54.32-56.10292Antarctic Ocean, Burdwood Bank4.934.1363.680.0male?
O37Graneledone yamanaANT-XXVII/3PS77/208-5Agassiz Trawl2011-02-11-54.32-56.10292Antarctic Ocean, Burdwood Bank4.934.1746.0130.0male?
O177Hapalochlaena lunulata-11.35137.62Pacific Ocean, Eastern Australia23.024.0Overath and von Boletzky (1974)approximate location
O181Hapalochlaena maculosa-38.72144.81Pacific Ocean, South-Eastern Australia14.022.5Tranter and Augustine (1973); Felix C Mark (2012)31.735.4Tranter and Augustine (1973)approximate location
O122Macroctopus maorumDecember 2012-44.83169.63New Zealand, Otago12.017.0Felix C Mark (2012)35.0
O11Megaleledone setebosANT-XXIII/8PS69/650Bottom Trawl2006-12-28-61.29-56.20330Antarctic Ocean, Elephant Island0.434.645.2female
O19Megaleledone setebosANT-XXIII/8PS69/676Bottom Trawl2007-01-02-62.18-60.79418Antarctic Ocean, Antarctic Peninsula0.434.680.0male
O9Megaleledone setebosANT-XXIII/8PS69/638Bottom Trawl2006-12-26-61.16-56.00149Antarctic Ocean, Elephant Island0.034.4160.0male
O189Octopus membranaceus-2.0087.00Indian Ocean28.032.0Nabhitabhata et al. (2005)approximate location
O182Octopus tetricus-31.99115.72Indian Ocean, Western Australia19.022.6Promboon et al. (2011)
O123Octopus vulgaris2012-01-0522.13114.17Pacific Ocean, China, Hongkong12.029.0Aguado Giménez and García García (2002); Caverivière et al. (1999); Miliou et al. (2005)Fish market
O124Octopus vulgaris201123.67128.86Pacific Ocean, Taiwan12.029.0Aguado Giménez and García García (2002); Caverivière et al. (1999); Miliou et al. (2005)
O153Octopus vulgarisSeptember 200842.493.14Mediterranean Sea, France, Banuyls12.029.0Aguado Giménez and García García (2002); Caverivière et al. (1999); Miliou et al. (2005)35.5
O154Octopus vulgarisSeptember 200842.493.14Mediterranean Sea, France, Banuyls12.029.0Aguado Giménez and García García (2002); Caverivière et al. (1999); Miliou et al. (2005)35.5
O27Pareledone aequipillaeANT-XXIII/8PS69/687Bottom Trawl2007-01-04-62.59-54.77263Antarctic Ocean, Antarctic Peninsula-0.934.561.6male
O28Pareledone aequipillaeANT-XXIII/8PS69/687Bottom Trawl2007-01-04-62.59-54.77263Antarctic Ocean, Antarctic Peninsula-0.934.547.9female
O31Pareledone aequipillaeANT-XXIII/8PS69/689Bottom Trawl2007-01-04-62.45-55.30224Antarctic Ocean, Antarctic Peninsula-0.834.532.3female
O13Pareledone aurataANT-XXIII/8PS69/657Bottom Trawl2006-12-29-61.24-55.82133Antarctic Ocean, Antarctic Peninsula0.334.353.7male
O68Pareledone aurataANT-XXVII/3PS77/217-5Agassiz Trawl2011-02-19-61.90-43.59408Antarctic Ocean, South Orkney Islands0.134.755.5049.0male
O118Pareledone charcoti2009-03-31-62.18-58.41Antarctic Ocean, King George Island-1.02.0Barnes et al. (2006)22.58
O155Pareledone charcoti-62.18-58.41Antarctic Ocean, King George Island-1.02.0Barnes et al. (2006)
O158Pareledone charcoti-62.18-58.41Antarctic Ocean, King George Island-1.02.0Barnes et al. (2006)
O69Pareledone cornutaANT-XXVII/3PS77/217-5Agassiz Trawl2011-02-19-61.90-43.59408Antarctic Ocean, South Orkney Islands0.134.752.7044.0female
O70Pareledone cornutaANT-XXVII/3PS77/217-6Bottom Trawl2011-02-19-62.00-44.20354Antarctic Ocean, South Orkney Islands0.134.791.5056.0female
O22Pareledone felixANT-XXIII/8PS69/680Bottom Trawl2007-01-02-62.40-61.40341Antarctic Ocean, Antarctic Peninsula0.434.657.4male
O74Pareledone felixANT-XXVII/3PS77/222-6Bottom Trawl2011-02-23-62.18-58.41459Antarctic Ocean, King George Island0.634.670.2048.0
O80Pareledone felixANT-XXVII/3PS77/222-6Bottom Trawl2011-02-23-62.18-58.41459Antarctic Ocean, King George Island0.634.610.9022.0female
O67Pareledone panchromaANT-XXVII/3PS77/217-5Agassiz Trawl2011-02-19-61.90-43.59408Antarctic Ocean, South Orkney Islands0.134.748.1040.0male
O102Pareledone prydzensisANT-XV/3PS77/308-1Bottom TrawlJanuary 1998-70.51-10.36224Antarctic Ocean, Eastern Weddel Sea-1.534.4approximate location
O93Pareledone prydzensisANT-XXVII/3PS77/308-1Bottom Trawl2012-04-04-70.51-10.35224Antarctic Ocean, Eastern Weddel Sea-1.534.410.3025.0male
O20Pareledone turquetiANT-XXIII/8PS69/677Bottom Trawl2007-01-02-62.18-60.55205Antarctic Ocean, Antarctic Peninsula-0.834.559.4male
O30Pareledone turquetiANT-XXIII/8PS69/689Bottom Trawl2007-01-04-62.45-55.30224Antarctic Ocean, Antarctic Peninsula-0.834.5120.0female
O16Pareledone turquetiANT-XXIII/8PS69/661Bottom Trawl2006-12-30-61.65-57.00467Antarctic Ocean, King George Island-0.934.565.8female