Evolution of respiratory adaptations in hydrothermal vent scales worms (Polynoidae)

Abstract

Hydrothermal vents are deep-sea ecosystems that are characterized by widely changing chemical and physical characteristics that are the result of the chaotic mixing of the hydrothermal fluid, rich in toxic compounds, such as sulfide and heavy metals, with low pH, high temperature and no oxygen; with the deep-sea water that contains no heavy metals, has a pH of ~7.8, low temperature and normal oxygen concentrations. Among others constraints, hypoxia and anoxia pose a serious problem for the fauna colonizing the hydrothermal ecosystems. Scale-worms (Polynoidea) living at hydrothermal vents are abundant, diverse and widely distributed in the range of chemical and thermal conditions. To obtain the benefits of living there (abundant local primary production), they need to cope with the harsh conditions that characterize these ecosystems. Respiratory pigments play a central function in the adaptation to hypoxia (uptake, transport and storage of the oxygen). Hydrothermal vent polynoids possess hemoglobins, a feature that clearly sets them aside from shallow water relatives. These hemoglobins are unique among annelids and their evolutionary history was the interest of this work. There are two main types of hemoglobins in hydrothermal vent polynoids: single- and tetra-domain globins. Although they are extracellular, both globins types are more closely related to intracellular globins that to the typical annelid extracellular ones. This indicates a distinct origin for these hemoglobins. We first studied the evolutionary history of the multi-domain gene hemoglobin and found out that it originates from the tandem duplication of a myoglobin/like ancestral. Both globin types possess residues in the heme pocket that have been shown to be responsible for the high oxygen affinity in the nematode Ascaris hemoglobin. These amino acids are also found in the globin from Harmothea, a non-vent-endemic species. This indicates that the adaptative value of these hemoglobins most likely resides in their expression at high levels in the body and did not require specific adaptations in the heme pocket in the lineage to give rise to all the vent species. In addition, some amino acid sites were shown to be under positive selection in some lineages. Some of these amino acids are located in the heme pocket where they will likely affect the functional properties and potentially provide protection against sulfide. The other amino acids under positive selection are located in areas where they will probably affect interactions between subunits for the single-domain globins, and between domains for the tetra-domain globins.