Molecular and functional adaptations in deep-sea hemoglobins

Hourdez, Stéphane; Weber, Roy E.

doi:10.1016/j.jinorgbio.2004.09.017

Cited by 71 publications

(35 citation statements)

References 83 publications

(135 reference statements)

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“…The other property, which is almost universal in these symbiotic molluscan groups, is the presence of tissue hemoglobins in the gills (Dando et al, 1985;Hourdez and Weber, 2005;Wittenberg, 1985;Wittenberg and Stein, 1995). Only the mytilids lack gill hemoglobins.…”

Section: Characteristics and Functioning Of Mollusc Chemoautotrophic mentioning

confidence: 99%

The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities

Childress

Girguis

2011

Journal of Experimental Biology

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SummaryWhile chemoautotrophic endosymbioses of hydrothermal vents and other reducing environments have been well studied, little attention has been paid to the magnitude of the metabolic demands placed upon the host by symbiont metabolism and the adaptations necessary to meet such demands. Here we make the first attempt at such an evaluation, and show that moderate to high rates of chemoautotrophic or methanotrophic metabolism impose oxygen uptake and proton equivalent elimination demands upon the hosts that are much higher than is typical for the non-symbiotic annelid, bivalve and gastropod lineages to which they are related. The properties of the hosts are described and compared to determine which properties are associated with and predictive of the highest rates. We suggest that the high oxygen demand of these symbionts is perhaps the most limiting flux for the symbioses. Among the consequences of such demands has been the widespread presence of circulating and/or tissue hemoglobins in these symbioses that are necessary to support high metabolic rates in thioautotrophic endosymbioses. We also compare photoautotrophic with chemoautotrophic and methanotrophic endosymbioses to evaluate the differences and similarities in physiologies. These analyses suggest that the high demand for oxygen by chemoautotrophic and methanotrophic symbionts is likely a major factor precluding their endosymbiosis with cnidarians. Supplementary material available online at

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Section: Characteristics and Functioning Of Mollusc Chemoautotrophic mentioning

confidence: 99%

The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities

Childress

Girguis

2011

Journal of Experimental Biology

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“…It has been calculated, based on an oxygen consumption rate independent of the partial pressure and starting with respiratory pigments fully saturated, that the bound oxygen could represent an autonomy of up to 1 h 30 min in the commensal hydrothermal vent polychaete Branchipolynoe seepensis (Hourdez and Weber 2005). This value only reaches 30 min in the coldseep polychaete Methanoaricia dendrobranchiata (Hourdez et al 2002).…”

Section: Obp As An Oxygen Storage Systemmentioning

confidence: 99%

“…All the species studied to date possess hemoglobin(s) in high concentrations, with a high affinity for oxygen when compared to shallow-water relatives, and a strong Bohr effect (Fig. 4, Hourdez and Weber 2005).…”

Section: Polychaetesmentioning

confidence: 99%

Adaptations to hypoxia in hydrothermal-vent and cold-seep invertebrates

Hourdez

Lallier

2006

Rev Environ Sci Biotechnol

102

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The deep sea harbors very unusual environments, such as hydrothermal vents and cold seeps, that illustrate an apparent paradox: the environmental conditions are very challenging and yet they display a high biomass when compared to the surrounding environment at similar depth. Hypoxia is one of the challenges that these species face to live there. Here, we review specific adaptations of their respiratory system that the species have developed to cope with hypoxia, at the morphological, physiological, and biochemical levels. Most studies to date deal with annelids and crustaceans, and trends can be drawn: development of ventilation and branchial surfaces to help with oxygen extraction, and an increase in finely tuned oxygen binding proteins to help with oxygen storage and transport. Beside these respiratory adaptations most animals have developed enhanced anaerobic capacities and specific ways to deal with sulfide.

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“…Despite this, only a limited number of studies have examined the full range of Hb genes, or functionally characterised their expression in bivalves (Terwilliger et al, 1983;Angelini et al, 1998;Hourdez & Weber, 2005;Decker et al, 2014). To better understand the evolution and expression of Hbs in bivalves, an investigation of Hb genes in two distantly related species of bivalves is performed here.…”

Section: Resultsmentioning

confidence: 99%

“…For example, the clam C. magnifica is found lodged into rock fissures outside hydrothermal vents and exposed to both deep-sea water and vent fluid meaning that it is frequently subject to chronic hypoxia (Berg, 1980). This species possesses an intracellular Hb with high O 2 affinity for carrying and transport required for its sustainability in such a challenging environment (Terwilliger et al, 1983;Scott & Fisher, 1995;Hourdez & Weber, 2005 (Kawano et al, 2003;Suzuki et al, 2000). Arcid bivalves are also frequently found in habitats with low levels of O 2 such as intertidal zones or deep-sea waters and often experience prolonged periods of hypoxia (Arp et al, 1984;Abele-Oeschger & Oeschger, 1995;Terwilliger, 1998;Weber & Vinogradov, 2001).…”

Section: Globin Gene Evolution In Hypoxic Environmentsmentioning

confidence: 99%

Characterisation of Duplicated Haemoglobin Genes in Bivalves

Klein¹

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Haemoglobins (Hbs) are found in virtually all phyla and are some of the most investigated proteins in biomedical sciences. These proteins exhibit an extraordinary diversity of form and function in invertebrate lineages. This provides a unique opportunity to explore the origin and evolution of Hbs yet little is known about their distribution, function and evolution in invertebrate lineages. To explore further the functions and evolution of those Hbs, recent transcriptome data for the Arcid bivalve Anadara trapezia is investigated here. This species shows the presence of duplicated Hb encoding genes suggesting that gene duplication may have been more extensive than previously thought in bivalves. This study tests the hypothesis that these duplicated genes show patterns of tissue specific expression and evidence of neofunctionalisation. This is shown here for at least three Hb encoding genes present in A. trapezia with strong tissue specific expression in haemolymph compared to other tissues. Furthermore, the expression of these genes remains unaffected by prolonged air exposure suggesting that neofunctionalisation may confer an evolutionary advantage to this bivalve. As well as the unique Hbs found in the bivalve order Arcoida, Hbs are also found in three other bivalve orders: Carditoida, Solemyoida and Veneroida. These four orders that possess Hbs provide compelling evidence for the independent evolution of these proteins in multiple bivalve lineages.To expand data on the distribution of Hbs in bivalves, a transcriptome sequence for Ctenoides ales in the order Limoida was generated in this project. Interrogation of the transcriptome shows the presence of at least three globin-like encoding genes including two Hb-like encoding genes providing preliminary evidence for another independent origin of Hb in a bivalve lineage. Overall, this study provides novel insights into the function, evolution and distribution of Hbs in bivalves by investigating two distantly related species. Results of this study are consistent with current theories that Hb diversity in bivalves is a result of repeated rounds of gene duplication providing the raw material for evolution. Investigation of hypoxic resistance also reinforces that greater expression of Hbs in haemolymph confers a physiological advantage suggesting that Hb would evolve more often in some lineages during adaptation to unfavourable environment conditions, particularlyAbstract ii hypoxia and prolonged air exposure.The finding of Hb-like encoding genes in another bivalve lineage also supports the evolution of this gene family through independent evolution and gene duplication, and gives insight into the distribution of globin genes in bivalves which is still poorly understood. The investigation of Hb genes in these bivalves also contributes to further understand the role of Hbs and provides potential novel insights for resistance in hypoxic environments, disease control and resistance to pollution in aquaculture.Abstract iii

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Molecular and functional adaptations in deep-sea hemoglobins

Cited by 71 publications

References 83 publications

The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities

The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities

Adaptations to hypoxia in hydrothermal-vent and cold-seep invertebrates

Characterisation of Duplicated Haemoglobin Genes in Bivalves

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