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Researchers Sequence, Analyze Genomes of Four Species of Mudskippers

NEW YORK (GenomeWeb) – Researchers from the State Key Laboratory of Agricultural Genomics in Shenzen, China, and elsewhere have sequenced the genomes of four species of mudskippers, getting a glimpse of the genomic changes they've accumulated to adapt to life on land.

Mudskippers are a family of amphibious fish that live on mudflats, though various species of the fish spend more time on land than others.

As researchers led by Qiong Shi reported in Nature Communications today, the mudskippers' genomes harbor changes to immune system, ammonia excretion, and vision-related genes that hint at how they've adapted to terrestrial living.

"Our analysis of four mudskipper genomes has provided insights into a variety of genetic changes that are likely associated with land adaptation of these amphibious fishes," Shi and colleagues wrote in their paper.

Understanding what changes these fish have undergone may also offer insight into how other vertebrates like tetrapods adapted earlier to living on land, the researchers noted.

"Since the intermediary forms that existed during the transition from aquatic lobe-finned fishes to terrestrial tetrapods are represented currently only in fossils, amphibious fishes offer a useful model for understanding genetic changes associated with the water-to-land transition of vertebrates," they added.

Shi and colleagues sequenced the genomes of four mudskippers — Boleophthalmus pectinirostris, Scartelaos histophorus, Periophthalmodon schlosseri, and Periophthalmus magnuspinnatus — using the Illumina HiSeq 2000 platform.

The researchers assembled the reads generated from those four mudskippers using SOAPdenovo2 into 0.966-, 0.720-, 0.683- and 0.715-gigabase genomes, respectively, and each was predicted to contain between 17,200 and 21,000 genes.

Based on these four genomes and eight additional vertebrate genomes, the researchers constructed the mudskipper phylogenetic tree. The four species formed a monophyletic clade that diverged from other teleosts some 140 million years ago. Within that clade, B. pectinirostris and S. histophorus form a sister group, as do P. schlosseri and P. magnuspinnatus, a finding the researchers say is unsurprising given that B. pectinirostris and S. histophorus are mostly aquatic, and P. schlosseri and P. magnuspinnatus are mostly terrestrial.

After diverging from other teleosts, mudskippers acquired changes that enabled them to adapt to mudflat living, changes that are reflected in their genomes, the researchers said.

They identified nearly 685 genes that are present in the mudskipper genome, but not in other teleosts. A number of these genes, they added, are enriched in immune domains.

For instance, mudskippers have four complete genes for toll-like receptor 13, which belongs to a family of innate immune receptors that can recognize bacterial 23S rRNA. The researchers suggested that the additional TLR13 genes and other additional immune-related genes mudskippers have may enable them to combat pathogens they encounter on land.

Additionally, since mudskippers can detoxify ammonia better than other aquatic species even though they don't rely on the ornithine-urea cycle that tetrapods use, Shi and colleagues examined nine genes that encode proteins involved in the ammonia excretion pathway in the gill.

Three proteins in this pathway appeared to be under significant positive selection in mudskippers — carbonic anhydrase 15 in both B. pectinirostris and P. magnuspinnatus, Na+/H+ exchanger 3 in B. pectinirostris, and glycosylated rhesus protein c 1 (Rhcg1) in P. magnuspinnatus. Positive selection on these genes, the researchers argued, suggests that they are involved in more efficient ammonia excretion in mudskipper gills.

Further, by comparing the mudskipper versions of Rhcg1 and predicting their three-dimensional shape, the researchers found that the P. magnuspinnatus Rhcg1 protein has an increased number of hydrophobic residues in the central pore, a change that they predicted eases the passage of ammonia through the pore.

Further, both the B. pectinirostris and P. magnuspinnatus mudskippers have lost an opsin subfamily, which the researchers suggested could be a response to increased exposure to ultraviolet light while on land.

And the mudskippers have fewer delta-class olfactory receptor-like genes than other teleost fish, indicating that they are less able to detect water-borne odorants. Likewise, compared to other fish, mudskippers have more VIR1 genes — vomeronasal receptors that bind air-borne chemicals — than VIR2 genes, which encode receptors that bind water-soluble chemicals.

To examine how these fish deal with desiccation and hypoxia on land, Shi and colleagues analyzed gene expression patterns in mudskipper brain, skin, liver, muscle, and gill tissues when exposed to air.

From their transcriptomic analyses, the researchers found that a number of genes are downregulated in those tissues, including ones involved in focal adhesion, ECM-receptor interaction, and cytokine-cytokine receptor interaction pathways. The downregulation of genes in these pathways, the researchers noted, has been associated with the inhibition of cell migration, stress fiber contraction, and proliferation. This, they said, may reflect an energy-saving strategy to cope with such hypoxic conditions.