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Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution.

ABSTRACT: Lampreys are representatives of an ancient vertebrate lineage that diverged from our own ?500 million years ago. By virtue of this deeply shared ancestry, the sea lamprey (P. marinus) genome is uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology. Here, we present the first lamprey whole-genome sequence and assembly. We note challenges faced owing to its high content of repetitive elements and GC bases, as well as the absence of broad-scale sequence information from closely related species. Analyses of the assembly indicate that two whole-genome duplications likely occurred before the divergence of ancestral lamprey and gnathostome lineages. Moreover, the results help define key evolutionary events within vertebrate lineages, including the origin of myelin-associated proteins and the development of appendages. The lamprey genome provides an important resource for reconstructing vertebrate origins and the evolutionary events that have shaped the genomes of extant organisms.

SUBMITTER: Smith JJ

PROVIDER: S-EPMC3709584 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution.

Smith Jeramiah J JJ Kuraku Shigehiro S Holt Carson C Sauka-Spengler Tatjana T Jiang Ning N Campbell Michael S MS Yandell Mark D MD Manousaki Tereza T Meyer Axel A Bloom Ona E OE Morgan Jennifer R JR Buxbaum Joseph D JD Sachidanandam Ravi R Sims Carrie C Garruss Alexander S AS Cook Malcolm M Krumlauf Robb R Wiedemann Leanne M LM Sower Stacia A SA Decatur Wayne A WA Hall Jeffrey A JA Amemiya Chris T CT Saha Nil R NR Buckley Katherine M KM Rast Jonathan P JP Das Sabyasachi S Hirano Masayuki M McCurley Nathanael N Guo Peng P Rohner Nicolas N Tabin Clifford J CJ Piccinelli Paul P Elgar Greg G Ruffier Magali M Aken Bronwen L BL Searle Stephen M J SM Muffato Matthieu M Pignatelli Miguel M Herrero Javier J Jones Matthew M Brown C Titus CT Chung-Davidson Yu-Wen YW Nanlohy Kaben G KG Libants Scot V SV Yeh Chu-Yin CY McCauley David W DW Langeland James A JA Pancer Zeev Z Fritzsch Bernd B de Jong Pieter J PJ Zhu Baoli B Fulton Lucinda L LL Theising Brenda B Flicek Paul P Bronner Marianne E ME Warren Wesley C WC Clifton Sandra W SW Wilson Richard K RK Li Weiming W

Nature genetics 20130224 4

Lampreys are representatives of an ancient vertebrate lineage that diverged from our own ∼500 million years ago. By virtue of this deeply shared ancestry, the sea lamprey (P. marinus) genome is uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology. Here, we present the first lamprey whole-genome sequence and assembly. We note challenges faced owing to its high content of repetitive elements and GC bases, as well as the abse ...[more]

PMID: 23435085

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Project description:The sea lamprey, Petromyzon marinus, is an anadromous, semelparous species that is vulnerable to endangered in parts of its native range due in part to loss of spawning habitat because of man-made barriers. The ability of lampreys to return to the ocean or estuary and search out alternative spawning river systems would be limited by their osmoregulatory ability in seawater. A reduction in tolerance to salinity has been documented in migrants, although the underlying mechanisms have not been characterized. We examined the capacity for marine osmoregulation in upstream spawning migrants by characterizing the physiological effects of salinity challenge from a molecular perspective. Estuarine-captured migrants held in freshwater (FW) for ∼1 week (short-term acclimation) or 2 months (long-term acclimation) underwent an incremental salinity challenge until loss of equilibrium occurred and upper thresholds of 25 and 17.5, respectively, occurred. Regardless of salinity tolerance, all lamprey downregulated FW ion-uptake mechanisms [gill transcripts of Na(+):Cl(-) cotransporter (NCC/slc12a3) and epithelial Na(+) channel (ENaC/scnn1) and kidney Na(+)/K(+)-ATPase (NKA) protein and activity but not transcript]. At their respective salinity limits, lamprey displayed a clear osmoregulatory failure and were unable to regulate [Na(+)] and [Cl(-)] in plasma and intestinal fluid within physiological limits, becoming osmocompromised. A >90% drop in haematocrit indicated haemolysis, and higher plasma concentrations of the cytosolic enzymes alanine aminotransferase, aspartate aminotransferase and lactate dehydrogenase indicated damage to other tissues, including liver. However, >80% of short-term FW-acclimated fish were able to osmoregulate efficiently, with less haemolysis and tissue damage. This osmoregulatory ability was correlated with significant upregulation of the secretory form of Na(+):K(+):2Cl(-) cotransporter (NKCC1/slc12a2) transcript levels and the re-emergence of seawater-type ionocytes detected through immunohistochemical NKA immunoreactivity in the gill, the central ionoregulatory organ. This work sheds light on the molecular and physiological limits to the potential return to seawater for lampreys searching for alternative FW systems in which to spawn.

Dataset Information

Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution.

Publications

Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution.

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