Genome-wide analysis of the Aquaporin gene family in reptiles

International Journal of Biological Macromolecules 126 (2019) 1093–1098

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International Journal of Biological Macromolecules journal homepage: http://www.elsevier.com/locate/ijbiomac

Genome-wide analysis of the Aquaporin gene family in reptiles Yu zang a,1, Jun Chen a,1, Huaming Zhong d,1, Jiayun Ren b,c, Wangfeng Zhao b, Qiang Man b, Shuai Shang a,b,c,⁎, Xuexi Tang a,⁎⁎ a

College of Marine Life, Ocean University of China, Qingdao, Shandong, China Shandong Key Laboratory of Eco-Environmental Science for the Yellow River Delta, China College of Biological and Environmental Engineering, Binzhou University, Binzhou, Shandong, China d College of Life Science, Qufu Normal University, Qufu, Shandong, China b c

a r t i c l e

i n f o

Article history: Received 15 October 2018 Received in revised form 2 January 2019 Accepted 2 January 2019 Available online 3 January 2019 Keywords: Aquaporin Reptile Terrestrial adaptation

a b s t r a c t Aquaporin (AQP) genes are widely distributed in plants, unicellular organisms, invertebrates and vertebrates. They play a critical role in the transport of water and other solutes across cell membranes. AQP genes have been identified and studied in many species but the AQPs of reptiles are unknown. Newly obtained genome assemblies provide an opportunity to identify the complete AQPs set and explore the evolutionary relationship of these genes. A total of 212 putative AQP genes were identified from 18 reptile species, including 20 partial genes and 192 intact genes. Phylogenetic results showed that 193 AQP genes could be classified into three major clades according to their subfamily. The divergence or phylogenetic distance between reptile AQP genes was closely related to traditional taxonomic groupings. Evolutionary analysis indicated the presence of positively selected sites in the AQP3 (P = 0.0104⁎⁎) and AQP7 (P = 0.0202⁎⁎) among land reptiles, suggesting their relationship to terrestrial environment adaptation. © 2019 Elsevier B.V. All rights reserved.

1. Introduction The maintenance of body fluid homeostasis is essential for the survival of all living organisms. Aquaporin (AQP), also referred to as water channels, are essential membrane proteins that are involved in the transport of water and other solutes across cell membranes. In addition to water transport, aquaporins are also involved in many other physiological functions, including urine concentration, brain swelling, neural signal transduction, skin moisturization, fat metabolism and exocrine gland secretion [1,2]. A total of 13 aquaporins (AQP0–12) have been identified in mammals and these can be divided into three subfamilies. AQP0, −1, −2, −4,-5, −6 and −8 are water-only aquaporins [3]. AQP3, −7, −9 and −10 transport both water and glycerol [3]. AQP11 and AQP12 belong to the super-aquaporins [4]. The aquaporin proteins consist of six transmembranes, five loops (A to E) and two characteristic internal tandem repeat motifs in loops B and E [5]. AQPs are widely distributed in plants, unicellular organisms, invertebrates and vertebrates and they have been studied in many species. 18 sequences structurally related to the four subfamilies of tetrapod

⁎ Correspondence to: S. Shang, College of Marine Life, Ocean University of China, Qingdao, Shandong, China. ⁎⁎ Corresponding author. E-mail addresses: [email protected] (S. Shang), [email protected] (X. Tang). 1 Equal contributors.

https://doi.org/10.1016/j.ijbiomac.2019.01.007 0141-8130/© 2019 Elsevier B.V. All rights reserved.

aquaporins were identified in the zebrafish [7], 13 AQP genes (AQP0–12) have been characterized in mammals [6], 17 AQP mRNAs have been identified in anurans and these are important for amphibian osmoregulation and transepithelial water transport [8]. However, the AQPs of reptiles remain largely unstudied. The terrestrial vertebrates, mammals, birds and reptiles share a common, but distant, evolutionary origin. During the early stages of tetrapod evolution, the mammals (Synapsida) split from the reptilian-avians (Archosauria) [9]. Extant reptiles comprise the Testudines, Rhynchocephalia, Squamata and Crocodilia [10,11]. They are poikilothermic amniotes that occupy various habitats, including marine, freshwater, flatlands and mountains [12]. Reptiles lack a urea habitus and do not have long medullary loops of Henle. Thus, they evolved a uric acid habitus to conserve water [9]. Water economy was a prerequisite for terrestrial reptile survival [9]. Semiquatic reptiles also faced the problem of the maintenance of body fluid homeostasis in their aqueous environment. We do not know if reptile AQP genes experienced different selection pressures in different habitats. The availability of whole genome sequences can provide insights into the evolutionary relationship of AQP genes in reptiles. We studied reptile AQP genes using genomewide analysis and explored their phylogenetic relationships and animo acid structure. We obtained the AQP genes from 18 reptile species. Four species were in the suborder Serpentes, five species in Lacertilia, five species in Testudines and four species in Crocodilia (Table S1). Then we performed a phylogenetic analysis of all intact AQP genes.

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2. Materials and methods

3. Results

2.1. Identification and syntenic analysis of AQP genes in reptiles

3.1. Aquaporin gene family in reptiles

Genome assemblies of 18 reptile species were obtained from the National Center for Biotechnology Information (NCBI, https://www.ncbi. nlm.nih.gov/) and GigaDB database (http://gigadb.org/). This genome information is shown in Table S1. The AQP amino acid sequences of the Anolis carolinensis, Chrysemys picta bellii, Python bivittatus and Chelonia mydas were used as queries to explore the genome sequences of the adder (Vipera berus), tuatara (Sphenodon punctatus), diamondback terrapin (Malaclemys terrapin) and green sea turtle (Lacerta bilineata). The TBLASTN and BLASTN in BLAST v2.2.23 were used for similarity searches in the four reptile genomes. An e-value of 10−5 was used as an initial cut-off to identify significant matches [2]. We conducted blast searches (cutoff e-value = 1e-10) in each Squamata genome by TBlastN. Hits ˂100 codons and overlapping sequences were abandoned. To determine the presence or absence of orthologs and to complete partial predicted genes sequences, the AQP genes were localized to chromosomes or scaffolds, and syntenic analysis was conducted for conserved flanking genes of each AQP gene in the reptiles.

Whole-genome sequence availability allowed for the identification and analysis of AQPs in reptiles. Totally, 212 putative aquaporin genes were identified from 18 reptile genomes, including 20 partial genes and 192 intact genes (Fig. 1). The number of AQP genes differed among the 18 reptile species. Syntenic analysis (Table S5) indicated that 22 AQP genes were absent in the reptiles. The AQP0 was absent in Terrapene mexicana triunguis, AQP1 was missing in Chelonia mydas, and the AQP6 gene was absent from four Crocodilia species. AQP7 was absent in Pogona vitticeps, Protobothrops mucrosquamatus, Thamnophis sirtalis and Gekko japonicas. AQP8 was absent in Anolis carolinensis, and AQP9 was absent in the Gavialis gangeticus, Crocodylus porosus and Anolis carolinensis. The AQP10 gene was absent in five Testudines species, AQP11 was absent in Gavialis gangeticus and Sphenodon punctatus and AQP12 was absent in the Sphenodon punctatus. The similarity of AQP genes among different reptiles is shown in Table S2. The similarity of the AQP 0–12 genes was 68.84–99.24%, 73.11–99.75%, 71.92–99.51%, 71.84–97.6%, 74.66–99.56%, 72.65–99.12%, 65.65–99.25%, 53.65–98.27%, 71.99–99.35%, 64.11–98.33%, 61.77–94.38%, 48.48–94.68%, 59.10–99.12%, respectively.

2.2. Phylogenetic analysis of AQP genes in reptiles To clarify relationships of the AQP genes in the 18 reptiles, we performed a phylogenetic analysis using Multiple Sequence Comparison by Log-Expectation (MUSCLE) [13] align the amino acid sequences of the AQP genes. The best fitting model was made using the Modelgenerator [14]. The phylogenetic relationship of the AQP genes in the 18 reptiles was constructed using the maximum likelihood (ML) method by Mega 7.0 [15] with 1000 bootstrap replications. The iTOL (http://itol.embl.de/help.cgi) was used to visualize the phylogenetic tree. 2.3. Evolutionary pressure analysis We used comparisons of nonsynonymous/synonymous substitution ratios (dN/dS) to quantify the natural selection [16]. Different types of selection were represented by different values: ω b 1 means purifying selection; ω N 1 indicates positive selection; ω = 1 means neutral selection. Selective pressure on AQP genes was conducted using the Codeml program implemented in the Phylogenetic Analysis by Maximum Likelihood (PAML 4.7) package [17] and Data Monkey Web Server (http:// www.datamonkey.org) [18]. Different ω ratio models (branch-site model) were used to determine if AQP genes in the terrestrial species have experienced positive selection. This model searched for the presence of positive selection on the terrestrial reptiles (Lacertilia and Serpents). We also used the branch-model to test for the presence of positive branches on the divergent clades of the 18 reptiles for the AQP genes. Then, we used M7 and M8 in PAML 4.7 to detect site-specific selection on the AQP genes. To ensure identification of positively selected sites in the 18 reptile species, three additional models were employed. Fixed-effect likelihood (FEL), single likelihood ancestor counting (SLAC) and random effect likelihood (REL) in Datamonkey were used to test for positive selection of AQP genes. 2.4. Structural modeling The predicted structural model of each AQP gene was built by CPHmodels-3.0 [19] (available at http://www.cbs.dtu.dk/services/ CPHmodels/). Then, we used the TMHMM to predict the transmembrane (TM) regions of the AQPs [20].

3.2. Phylogenetic analysis of AQP genes We aligned only intact and long partial AQP gene sequences; the short partial genes were discarded. A total of 193 AQP genes were used to build a phylogenetic tree. The results showed that the 193 aquaporin genes were classified into three major clades. AQP11 and AQP12 clustered together; AQP3,-7, −9 and −10 clustered and AQP0, −1, −2, −4, −5, −6 and AQP8 clustered. These relationships were consistent with the three subfamilies (Fig. 2). Within each subfamily, the AQP genes exhibited between-species phylogenetic relationships (Fig. 2). The divergence or phylogenetic distance between the reptile AQP genes was closely related to the traditional taxonomic groupings. For example, most of the AQP genes of the Crocodilia clustered together, the AQP genes of the Testudines clustered together and the AQP genes of the Squamata clustered together.

3.3. Characteristics of positively selected sites in the AQP genes of reptiles We used three methods to identify possible positively selected sites (Table 1). Three common positively selected sites were identified in AQP4. Two common positively selected sites were identified in AQP2, −9 and −12. One common positively selected site was identified in AQP1 and AQP6. No common positively selected sites were identified in AQP0, −3, −5, −7, −8, −10 and −11.

3.4. Positive selection of AQP genes in terrestrial species Different ω ratio models were used to determine if AQP genes in the terrestrial species have experienced positive selection. The ω value of AQP0 (P = 0.031⁎⁎), AQP7 (P = 0.0000028⁎⁎), AQP9 (P = 0.00022⁎⁎) and AQP11 (P = 0.0014⁎⁎) in different branches exhibited variable ω ratios (Table 2). The remaining AQP genes showed no variable ω ratio in the different branches (Table 2). The results of branch-site model A (Table 3) revealed evidence of positive selection on AQP genes among the reptile lineages, as indicated by substitutions in specific sites. Significantly positive AQP3 (P = 0.0104⁎⁎), AQP7 (P = 0.0202⁎⁎) and AQP11 (P = 0.00705⁎⁎) were present in the land species. No significant positive sites were detected in the remaining AQP genes among the tested lineages.

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Fig. 1. The divergence and AQP genes of the 18 reptile species.

Fig. 2. Phylogenetic tree of AQP genes of the reptilian species. A total of 193 AQP genes were used in a phylogenetic tree constructed by MEGA 7.0 with 1000 bootstrap replications and the best fitting model Jones-Taylor-Thornton (JTT) + G + I + F. The phylogenetic tree was divided into three major clades according to the subfamily of the AQP genes. Different AQP genes are marked in different colors.

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Table 1 Test for positive selection in reptilian AQP genes using site models. Gene

No. of LnL M7 species

LnL M8

AQP0 AQP1 AQP2

15 15 18

−3242.03 −3242.02 −4293.35 −4273.39 −4635.61 −4629.50

AQP3

16

−5235.30 −5227.14

AQP4

17

−4488.49 −4479.68

AQP5

18

−3756.77 −3751.57

AQP6 AQP7 AQP8

12 10 16

−3183.88 −3182.44 −2659.93 −2659.93 −3709.26 −3704.59

AQP9

13

AQP10 AQP11 AQP12

10 14 17

LRT P-value

M8

−4996.32 −4994.84

P = 0.998 P ≪ 0.01 P= 0.0022 P= 0.00028 P= 0.00015 P= 0.0055 P = 0.24 P=1 P= 0.0094 P = 0.23

−3125.18 −3122.39 −3605.30 −3604.87 −4815.53 −4813.14

P = 0.061 P = 0.64 P = 0.916

SLAC FEL

REL

Total no. of sites

0 36, 45, 120, 133, 137, 206, 219 37

0 0 0

0 137 201

0 0 37, 42, 158, 201

0 1 2

132, 128, 140

0

0

77

0

40, 117, 122, 127, 161, 184, 209, 234, 256, 276 111, 197

0

21, 127

40, 127, 234, 238

3

0

9

0

0

122, 123, 196 283 130

0 0 0

73, 123 56, 254 0

0 0 0

1 0 0

219, 276

0

127

2

239, 288 138 23, 168, 245

0 0 222

120 12, 73, 199 12, 79, 82, 222, 241, 257, 282, 283, 299

127, 132, 219, 268, 276, 280, 299 0 0 296, 299, 300,301

0 0 2

Note: Sequences of positively selected sites are based on Anolis carolinensis amino-acid numbers, common positively selected sites were marked with underline, bold.

4. Discussion AQP genes are important for normal functioning of vertebrates. They facilitate permeation of small molecules and regulate cell functions such as energy metabolism, proliferation, osmolarity, migration, adhesion, and differentiation. Reptiles have played a crucial role in the evolution of terrestrial vertebrates. AQP genes are important for reptile water conservation systems and have enabled adaptation to life in terrestrial environments. However, little evolutionary analysis or molecular characterization of reptile AQP genes has been conducted. We studied the phylogenetic relationships and molecular evolution of AQP genes in 18 reptiles. AQP genes from the speckled rattlesnake, adder, tuatara

Table 2 Tests for positive selection in divergent clades of AQP genes with branch models. Gene AQP0 AQP1 AQP2 AQP3 AQP4 AQP5 AQP6 AQP7 AQP8 AQP9 AQP10 AQP11 AQP12

Model Model 0 Model 2 Model 0 Model 2 Model 0 Model 2 Model 0 Model 2 Model 0 Model 2 Model 0 Model 2 Model 0 Model 2 Model 0 Model 2 Model 0 Model 2 Model 0 Model 2 Model 0 Model 2 Model 0 Model 2 Model 0 Model 2

np 30 31 30 31 36 37 32 33 34 35 36 37 24 25 20 21 32 33 26 27 20 21 29 28 34 35

LnL −3271.80 −3269.48 −4407.30 −4407.31 −4693.63 −4693.63 −5379.96 −5379.94 −4567.43 −4567.37 −3817.59 −3817.27 −3231.40 −3231.40 −2683.55 −2672.58 −3765.47 −3765.47 −5075.02 −5068.20 −3203.52 −3203.49 −3679.02 −3673.89 −4867.18 −4867.29

Note: ⁎ represents P b 0.05; ⁎⁎ P b 0.01.

LRT P-value

ω for branch

0.031⁎⁎ 0.00010 0.988 0.0812 0.987 0.11131 0.829 0.09641 0.7278 0.17448 0.4197 0.10175 0.9921 0.0000028⁎⁎

0.21955 0.00258

0.9864 0.00022⁎⁎

0.09967 0.03036

0.81267 0.0014⁎⁎

0.10486 999

0.6434 0.2875

and Western Green Lizard were studied for the first time. The similarity of reptile AQP gene sequences ranged from 48.48%–99.75% at the amino acid level, indicating that the AQP genes were species-specific among the 18 reptile species. Previous studies have found that the repertoire of AQP genes differs among different species [21]. For example, AQP10 is a pseudogene in mice [22] and the orthologs of AQP2, −6, −8 and −10 are missing in chickens [23]. The AQP2, −5 and −6 were lacking in five species of Teleostei [24]. Seventeen AQP genes have been found in anurans [8]. AQP1, −2, −3, and −4 have been identified and characterized in avian kidneys. Gene sequences of AQP5, −7, −8, −9, −11, and −12 have been reported in birds [25]. Our result provide the first analysis of reptile AQPs and the repertoire of these also varies among different species. AQP6 genes were absent in four Crocodilia species. AQP7 was absent in Pogona vitticeps, Protobothrops mucrosquamatus, Thamnophis sirtalis and Gekko japonicas. AQP10 was absent in five Testudines species. Most reptiles had ten AQP genes, the Gavialis gangeticus had the least number (9) of AQP genes. One explanation for the different number of AQP genes may involve the functional complementation in reptiles. Another explanation may be that the loss of certain AQP genes is species specific and related to adaption to different habitats. There is evidence for independent intrachromosomal duplications in Hyperoartia, Actinopterygii, Sarcopterygii and Chondrichthyes [24]. We found that the AQP genes clustered into three major clades corresponding to their subfamilies. This indicated that the AQP genes are conserved among the reptiles. AQP0, −1, −2, −4, −5 and −6 have been classified as waterselective classical AQP genes. AQP8 is an ammoniaporin which transports water, urea and ammonia. AQP3, −7, −9 and −10 are classical aquaglyceroporins which transport water, urea, arsenic and polyols. AQP11 and AQP12 are classified as unorthodox aquaporins [7,24,26–30]. Common positively selected sites were found in AQP1, −2, −4, −6, −9 and −12. Most of these were located in the outside region (Table 4). AQP0 is specifically expressed in the fibers of the ocular lens and designated MIP, which is involved in the physiological functioning of the lens [4]. AQP2, −5, and −6 channels have important functions in the skin, urinary bladder, salt glands, and kidneys of amphibians, sauropsids, and mammals [25]. AQP2 is present in the apical membrane of the cortex in birds [9]. AQP2 and AQP6 also play important roles in adaptation to terrestrial environments [24], and the predicted positively selected sites in AQP2 and AQP6 may be important

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Table 3 Selective pressure analyses of AQP genes in reptiles using branch-site models. Gene

Model

np

LnL

AQP0

Model A Model A null Model A Model A null Model A Model A null Model A Model A null Model A Model A null Model A Model A null Model A Model A null Model A Model A null Model A Model A null Model A Model A null Model A Model A null Model A Model A null Model A Model A null

33 32 33 32 39 38 32 33 37 36 39 38 24 25 23 22 35 34 29 28 23 22 31 30 37 36

−3269.24 −3263.24 −4297.29 −4297.29 −4647.61 −4647.61 −5287.39 −5290.66 −4488.99 −4488.99 −3773.28 −3773.28 −3191.07 −3191.07 −2665.67 −2665.67 −3728.40 −3728.40 −5017.87 −5017.87 −3157.85 −3157.85 −3634.23 −3637.86 −4816.98 −4816.98

AQP1 AQP2 AQP3 AQP4 AQP5 AQP6 AQP7 AQP8 AQP9 AQP10 AQP11 AQP12

LRT P-value

Positive sites

1 NA 1 NA 1 NA

0.0104⁎⁎

157⁎⁎, 227, 276

0.9941 NA 1 NA 0.9948 NA

0.0202⁎⁎

7, 174, 185, 277 1 NA 1 NA 0.9941 NA

0.00705⁎⁎

49, 94, 97, 102, 104, 105, 110, 111, 116⁎⁎, 126⁎, 130, 131, 159⁎, 162, 163, 169, 185

0.9984 NA

Note: Sequences of positively selected sites are based on Anolis carolinensis amino-acid numbers. ⁎ represents P b 0.05 ⁎⁎ represents P b 0.01.

for water conservation in reptiles. Kong et al. found that expression of AQP4 in the central nervous system was important for maintaining water and ion homeostasis [32]. When expressed in adult neural stem cells, AQP4 was essential for regulating cell proliferation, migration and differentiation [32]. In this study, three common positively selected sites were identified in the AQP4 gene, which may be important for maintaining water and ion homeostasis in reptiles. AQP9 functions as an aquaglyceroporin with a broad substrate spectrum [33], including water, urea, arsenic trioxide, monomethylarsenous acid and dimethylarsenic acid. The ω of AQP9 (P = 0.00022**) in different branches exhibited a variable ω ratio. Due to the broad substrate spectrum of AQP9 we believe that it is important for water conservation in reptiles. AQP2, −5 and −6 are specific to the lineage that gave rise to the terrestrial radiation of animals and this implies their pivotal roles in terrestrial radiation [24]. Our research indicated the presence of positively selected sites in AQP3, −7 and −11 among reptile land species, suggesting adaptations to terrestrial environments. Verkman demonstrated that AQP3 was involved in biology and cell proliferation [26], Rachid et al. suggested that AQP3 was involved in hydration of the epidermis

by preventing the formation of an osmotic gradient across epidermal layers [34]. We think that the predicted positively selected sites (157**, 227 and 276) of AQP3 may help confer high water permeability to viable layers of the epidermis which would be an adaptation to terrestrial environments. Iena et al. showed that AQP7 was expressed in a wide range of tissues, facilitated the transport of glycerol across cell membranes and was important in modulating whole body energy metabolism [35]. We identified four positively selected sites (7174, 185 and 277) using the branch-site model, which might also be reptile adaptations to terrestrial environments. Northern blot analysis of rats showed that AQP11 was expressed in the testis, kidney, liver and brain, and functioned as an efficient water channel [36]. Yoshiyuki et al. found that AQP11 was essential for the proximal tubular function in mice [37]. Our research revealed 17 positively selected sites in land and semiaquatic reptiles. This suggests an important role of AQP11 in land reptiles. But the similarity of AQP11 among reptile species ranged from 48.48% to 94.68% and the length of AQP11 gene sequences was also variable. Thus, we speculate that the evolutionary significance of AQP11 for land adaption remains unclear. 5. Conclusions

Table 4 Location of the common positively selected sites of AQP genes in reptiles. Gene

AQP0 AQP1 AQP2 AQP3 AQP4 AQP5 AQP6 AQP7 AQP8 AQP9 AQP10 AQP11 AQP12

Location of the common positively selected sites Inside

Transmembrane helix

Outside

0 0 0 0 1 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 1 0 0 0

0 1 2 0 2 0 1 0 0 1 0 0 2

We explored the phylogenetic relationship and evolution of AQP genes in 18 reptile species. A total of 212 putative AQP genes were identified. Evolutionary analysis indicated the presence of positively selected sites in AQP3 (P = 0.0104⁎⁎) and AQP7 (P = 0.0202⁎⁎) among the land reptiles, suggesting their involvement in adaptation to terrestrial environments. This study revealed valuable information regarding AQP genes in reptiles and provided insights into terrestrial adaptation. Supplementary data to this article can be found online at https://doi. org/10.1016/j.ijbiomac.2019.01.007. Acknowledgment This work was financially supported by the National Natural Science Foundation of China (No. 41476091, U1806213) and the Doctoral scientific fund of Binzhou University (20118Y17).

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