Biochemical Adaptations of Notothenioid Fishes: Comparisons Between Cold Temperate South American and New Zealand Species and Antarctic Species☆ ⁎ Zulema L

Comparative Biochemistry and Physiology, Part A 147 (2007) 799–807 www.elsevier.com/locate/cbpa Review Biochemical adaptations of notothenioid fishes: Comparisons between cold temperate South American and New Zealand species and Antarctic species☆ ⁎ Zulema L. Coppes Petricorena a, , George N. Somero b a Faculty of Chemistry — Montevideo, Uruguay b Hopkins Marine Station, Department of Biological Sciences, Stanford University, Pacific Grove, CA 93950-3094, USA Received 17 June 2006; received in revised form 17 September 2006; accepted 29 September 2006 Available online 5 December 2006 Abstract Fishes of the perciform suborder Notothenioidei afford an excellent opportunity for studying the evolution and functional importance of diverse types of biochemical adaptation to temperature. Antarctic notothenioids have evolved numerous biochemical adaptations to stably cold waters, including antifreeze glycoproteins, which inhibit growth of ice crystals, and enzymatic proteins with cold-adapted specific activities (kcat values) and substrate binding abilities (Km values), which support metabolism at low temperatures. Antarctic notothenioids also exhibit the loss of certain biochemical traits that are ubiquitous in other fishes, including the heat-shock response (HSR) and, in members of the family Channichthyidae, hemoglobins and myoglobins. Tolerance of warm temperatures is also truncated in stenothermal Antarctic notothenioids. In contrast to Antarctic notothenioids, notothenioid species found in South American and New Zealand waters have biochemistries more reflective of cold-temperate environments. Some of the contemporary non-Antarctic notothenioids likely derive from ancestral species that evolved in the Antarctic and later “escaped” to lower latitude waters when the Antarctic Polar Front temporarily shifted northward during the late Miocene. Studies of cold-temperate notothenioids may enable the timing of critical events in the evolution of Antarctic notothenioids to be determined, notably the chronology of acquisition and amplification of antifreeze glycoprotein genes and the loss of the HSR. Genomic studies may reveal how the gene regulatory networks involved in acclimation to temperature differ between stenotherms like the Antarctic notothenioids and more eurythermal species like cold-temperate notothenioids. Comparative studies of Antarctic and cold-temperate notothenioids thus have high promise for revealing the mechanisms by which temperature-adaptive biochemical traits are acquired – or through which traits that cease to be of advantage under conditions of stable, near-freezing temperatures are lost – during evolution. © 2006 Elsevier Inc. All rights reserved. Keywords: Antarctica; Antifreeze glycoproteins; Heat-shock response; Notothenioid; Temperature adaptation Contents 1. Geological and oceanographic drivers of evolution in notothenioid fishes . ............................ 800 2. Characteristics of the Antarctic fish fauna: the suborder Notothenioidei . ............................ 800 3. Non-Antarctic notothenioids ..................................................... 801 4. Antifreeze glycoproteins ....................................................... 801 5. Gene loss in stably cold waters: the heat-shock response ...................................... 802 ☆ This paper is part of the 3rd special issue of CBP dedicated to The Face of Latin American Comparative Biochemistry and Physiology organized by Marcelo Hermes-Lima (Brazil) and co-edited by Carlos Navas (Brazil), Rene Beleboni (Brazil), Rodrigo Stabeli (Brazil), Tania Zenteno-Savín (Mexico) and the editors of CBP. This issue is dedicated to the memory of two exceptional men, Peter L. Lutz, one of the pioneers of comparative and integrative physiology, and Cicero Lima, journalist, science lover and Hermes-Lima's dad. ⁎ Corresponding author. E-mail address: [email protected] (Z.L. Coppes Petricorena). 1095-6433/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpa.2006.09.028 800 Z.L. Coppes Petricorena, G.N. Somero / Comparative Biochemistry and Physiology, Part A 147 (2007) 799–807 6. Temperature adaptation of enzymatic proteins............................................. 803 7. Structural adaptations of muscle fibres: relationship between diameter and number ......................... 804 8. Genetics of notothenioids: what has been lost during evolution in stably cold waters? ........................ 805 Acknowledgements ............................................................. 805 References ................................................................. 805 1. Geological and oceanographic drivers of evolution in The stably cold and oxygen-rich waters found southward of notothenioid fishes the APF would be expected to serve as important effectors of evolution in the Antarctic marine biota. One would anticipate Fishes of the perciform suborder Notothenioidei afford an that during the approximately 40 million years of existence of excellent study system for examining how large-scale geologi- the ACC and APF, adaptations to temperature would have led to cal and oceanographic processes serve as drivers of evolution to extensive differentiation of organisms endemic to waters to the the physical environment. The formation of the Southern north or south of the APF. Studies of the major group of Ocean, which surrounds Antarctica and includes the great Antarctic fishes, members of the perciform suborder Notothe- embayments of the Weddell and Ross Seas, was marked by the nioidei, and their cold-temperate relatives in South America and creation of a large mass of water – the planet's fourth largest New Zealand, show this to be the case. The biochemical ocean – that is uniquely cold and thermally stable. The Southern differences between polar and cold-temperate notothenioids Ocean is covered by sea ice during the winter, from the reflect the gain of important adaptive traits in both groups and Antarctic coastline northward to approximately 60°S (Gordon, the loss of traits no longer needed for life in stably cold waters in 1988, 1999, 2003). The Southern Ocean is much younger than Antarctic species. This short review discusses these key other oceans because of its origins as a result of plate tectonic differences and suggests new lines of studies, many of which activities over the past approximately 40–60 million years. Two are based on the new genomic technologies now becoming key events in the formation of the Southern Ocean were the available for fishes, that may contribute importantly to our opening of the Drake Passage between South America and the understanding of molecular evolution in protein-coding and Antarctic continent, which recent analyses suggest took place gene regulatory components of the genome. approximately 41 million years ago, and the formation of the Tasmanian Gateway, which is now thought to have occurred a 2. Characteristics of the Antarctic fish fauna: the suborder few millions years after the opening of the Drake Passage Notothenioidei (Scher and Martin, 2006). The separation of these southern landmasses permitted formation of the Antarctic Circumpolar Beginning in the early Miocene (25–22 million years ago), Current (ACC), the oceanographic feature of the Southern the Antarctic shelf was subject to a series of tectonic and Ocean that plays a pivotal role in establishing the thermal oceanographic events that undoubtedly altered faunal composi- conditions that have driven evolution of the Antarctic biota tion. Antarctica gradually became isolated and colder and (Eastman, 1993). The ACC is the ocean's largest current. It is expansion of the ice sheet led to destruction and disturbance of 21,000 km in length and transports 130 million cubic meters of inshore habitat by ice, as a consequence of repeated groundings water per second — 100 times the flow of all the world's rivers of parts of the ice sheet as far as the shelf break (Clarke and (Gordon, 1999). The Antarctic Polar Front (APF), the northern Johnston, 1996; Anderson, 1999). Loss of habitat and changes border of the ACC between 50°S and 60°S, prevents mixing of in the trophic structure of the ecosystem probably led to the the waters of the Southern Ocean with those of the Indian, local extinction of many of the Eocene components of the fish Pacific and Atlantic oceans. The APF thus acts as a cold “wall” fauna. Thus, the diversity of the fauna was reduced and, as that inhibits mixing of the fauna of the cold temperate ocean to Antarctica became increasingly isolated, new niches became the north with the cold-adapted fauna of the Southern Ocean. available to groups that were diversifying in situ (notothe- However, this “wall” may not be impenetrable at all depths, for nioids) or immigrating into (liparids and zoarcids) this recent studies suggest that “leakage” of invertebrates may occur developing cold-water ecosystem (Eastman, 2005). Little is in deep water (Clarke et al., 2005). known, however, about when the fauna became modern in Sea temperatures of the Southern Ocean have been well taxonomic composition. below 5 °C for 10 to 14 MY and they presently approach −2°C The first Antarctic notothenioids to be reported in the at the more southerly boundaries of the shelf (Littlepage, 1965). literature were collected near Kerguelen Island during the Annual variation in temperature of McMurdo Sound waters expedition of the Erebus and Terror under command of Sir (78°S) is between −1.9 °C and −0.5 °C (Hunt et al., 2003). In James Clark Ross (1839–1843). Prior

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