The Greenland shark Somniosus microcephalus -Hemoglobins and ligand-binding properties

Roberta Russo; Daniela Giordano; Gianluca Paredi; Francesco Marchesani; Lisa Milazzo; Giovanna Altomonte; Pietro Del Canale; Stefania Abbruzzetti; Paolo Ascenzi; Guido Di Prisco; Cristiano Viappiani; Angela Fago; Stefano Bruno; Giulietta Smulevich; Cinzia Verde

doi:10.1371/journal.pone.0186181

The Greenland shark Somniosus microcephalus -Hemoglobins and ligand-binding properties

Roberta Russo, Daniela Giordano, Gianluca Paredi, Francesco Marchesani, Lisa Milazzo, Giovanna Altomonte, Pietro Del Canale, Stefania Abbruzzetti, Paolo Ascenzi, Guido Di Prisco, Cristiano Viappiani, Angela Fago, Stefano Bruno, Giulietta Smulevich, Cinzia Verde^*

^*Corresponding author af dette arbejde

Institut for Biologi - Zoofysiologi

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

4 Citationer (Scopus)

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Abstract

A large amount of data is currently available on the adaptive mechanisms of polar bony fish hemoglobins, but structural information on those of cartilaginous species is scarce. This study presents the first characterisation of the hemoglobin system of one of the longest-living vertebrate species (392 ± 120 years), the Arctic shark Somniosus microcephalus. Three major hemoglobins are found in its red blood cells and are made of two copies of the same α globin combined with two copies of three very similar β subunits. The three hemoglobins show very similar oxygenation and carbonylation properties, which are unaffected by urea, a very important compound in marine elasmobranch physiology. They display identical electronic absorption and resonance Raman spectra, indicating that their heme-pocket structures are identical or highly similar. The quaternary transition equilibrium between the relaxed (R) and the tense (T) states is more dependent on physiological allosteric effectors than in human hemoglobin, as also demonstrated in polar teleost hemoglobins. Similar to other cartilaginous fishes, we found no evidence for functional differentiation among the three isoforms. The very similar ligand-binding properties suggest that regulatory control of O ₂ transport may be at the cellular level and that it may involve changes in the cellular concentrations of allosteric effectors and/or variations of other systemic factors. The hemoglobins of this polar shark have evolved adaptive decreases in O ₂ affinity in comparison to temperate sharks.

Originalsprog	Engelsk
Artikelnummer	e0186181
Tidsskrift	P L o S One
Vol/bind	12
Nummer	10
Antal sider	24
ISSN	1932-6203
DOI	https://doi.org/10.1371/journal.pone.0186181
Status	Udgivet - 12 okt. 2017

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10.1371/journal.pone.0186181Licens: CC BY

journal.pone.0186181Forlagets udgivne version, 4,16 MBLicens: CC BY

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Russo, R., Giordano, D., Paredi, G., Marchesani, F., Milazzo, L., Altomonte, G., Del Canale, P., Abbruzzetti, S., Ascenzi, P., Di Prisco, G., Viappiani, C., Fago, A., Bruno, S., Smulevich, G., & Verde, C. (2017). The Greenland shark Somniosus microcephalus -Hemoglobins and ligand-binding properties. P L o S One, 12(10), Artikel e0186181. https://doi.org/10.1371/journal.pone.0186181

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title = "The Greenland shark Somniosus microcephalus -Hemoglobins and ligand-binding properties",

abstract = "A large amount of data is currently available on the adaptive mechanisms of polar bony fish hemoglobins, but structural information on those of cartilaginous species is scarce. This study presents the first characterisation of the hemoglobin system of one of the longest-living vertebrate species (392 ± 120 years), the Arctic shark Somniosus microcephalus. Three major hemoglobins are found in its red blood cells and are made of two copies of the same α globin combined with two copies of three very similar β subunits. The three hemoglobins show very similar oxygenation and carbonylation properties, which are unaffected by urea, a very important compound in marine elasmobranch physiology. They display identical electronic absorption and resonance Raman spectra, indicating that their heme-pocket structures are identical or highly similar. The quaternary transition equilibrium between the relaxed (R) and the tense (T) states is more dependent on physiological allosteric effectors than in human hemoglobin, as also demonstrated in polar teleost hemoglobins. Similar to other cartilaginous fishes, we found no evidence for functional differentiation among the three isoforms. The very similar ligand-binding properties suggest that regulatory control of O 2 transport may be at the cellular level and that it may involve changes in the cellular concentrations of allosteric effectors and/or variations of other systemic factors. The hemoglobins of this polar shark have evolved adaptive decreases in O 2 affinity in comparison to temperate sharks.",

keywords = "RESONANCE RAMAN-SPECTRA, AMINO-ACID SEQUENCE, OXYGEN-BINDING, CARTILAGINOUS FISH, HETERODONTUS-PORTUSJACKSONI, ELASMOBRANCH HEMOGLOBIN, STRETCHING FREQUENCIES, MOLECULAR ADAPTATIONS, QUATERNARY STRUCTURES, NOTOTHENIOID FISHES",

author = "Roberta Russo and Daniela Giordano and Gianluca Paredi and Francesco Marchesani and Lisa Milazzo and Giovanna Altomonte and {Del Canale}, Pietro and Stefania Abbruzzetti and Paolo Ascenzi and {Di Prisco}, Guido and Cristiano Viappiani and Angela Fago and Stefano Bruno and Giulietta Smulevich and Cinzia Verde",

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T1 - The Greenland shark Somniosus microcephalus -Hemoglobins and ligand-binding properties

AU - Russo, Roberta

AU - Giordano, Daniela

AU - Paredi, Gianluca

AU - Marchesani, Francesco

AU - Milazzo, Lisa

AU - Altomonte, Giovanna

AU - Del Canale, Pietro

AU - Abbruzzetti, Stefania

AU - Ascenzi, Paolo

AU - Di Prisco, Guido

AU - Viappiani, Cristiano

AU - Fago, Angela

AU - Bruno, Stefano

AU - Smulevich, Giulietta

AU - Verde, Cinzia

PY - 2017/10/12

Y1 - 2017/10/12

N2 - A large amount of data is currently available on the adaptive mechanisms of polar bony fish hemoglobins, but structural information on those of cartilaginous species is scarce. This study presents the first characterisation of the hemoglobin system of one of the longest-living vertebrate species (392 ± 120 years), the Arctic shark Somniosus microcephalus. Three major hemoglobins are found in its red blood cells and are made of two copies of the same α globin combined with two copies of three very similar β subunits. The three hemoglobins show very similar oxygenation and carbonylation properties, which are unaffected by urea, a very important compound in marine elasmobranch physiology. They display identical electronic absorption and resonance Raman spectra, indicating that their heme-pocket structures are identical or highly similar. The quaternary transition equilibrium between the relaxed (R) and the tense (T) states is more dependent on physiological allosteric effectors than in human hemoglobin, as also demonstrated in polar teleost hemoglobins. Similar to other cartilaginous fishes, we found no evidence for functional differentiation among the three isoforms. The very similar ligand-binding properties suggest that regulatory control of O 2 transport may be at the cellular level and that it may involve changes in the cellular concentrations of allosteric effectors and/or variations of other systemic factors. The hemoglobins of this polar shark have evolved adaptive decreases in O 2 affinity in comparison to temperate sharks.

AB - A large amount of data is currently available on the adaptive mechanisms of polar bony fish hemoglobins, but structural information on those of cartilaginous species is scarce. This study presents the first characterisation of the hemoglobin system of one of the longest-living vertebrate species (392 ± 120 years), the Arctic shark Somniosus microcephalus. Three major hemoglobins are found in its red blood cells and are made of two copies of the same α globin combined with two copies of three very similar β subunits. The three hemoglobins show very similar oxygenation and carbonylation properties, which are unaffected by urea, a very important compound in marine elasmobranch physiology. They display identical electronic absorption and resonance Raman spectra, indicating that their heme-pocket structures are identical or highly similar. The quaternary transition equilibrium between the relaxed (R) and the tense (T) states is more dependent on physiological allosteric effectors than in human hemoglobin, as also demonstrated in polar teleost hemoglobins. Similar to other cartilaginous fishes, we found no evidence for functional differentiation among the three isoforms. The very similar ligand-binding properties suggest that regulatory control of O 2 transport may be at the cellular level and that it may involve changes in the cellular concentrations of allosteric effectors and/or variations of other systemic factors. The hemoglobins of this polar shark have evolved adaptive decreases in O 2 affinity in comparison to temperate sharks.

KW - RESONANCE RAMAN-SPECTRA

KW - AMINO-ACID SEQUENCE

KW - OXYGEN-BINDING

KW - CARTILAGINOUS FISH

KW - HETERODONTUS-PORTUSJACKSONI

KW - ELASMOBRANCH HEMOGLOBIN

KW - STRETCHING FREQUENCIES

KW - MOLECULAR ADAPTATIONS

KW - QUATERNARY STRUCTURES

KW - NOTOTHENIOID FISHES

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U2 - 10.1371/journal.pone.0186181

DO - 10.1371/journal.pone.0186181

M3 - Journal article

C2 - 29023598

SN - 1932-6203

VL - 12

JO - P L o S One

JF - P L o S One

IS - 10

M1 - e0186181

ER -

The Greenland shark Somniosus microcephalus -Hemoglobins and ligand-binding properties

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