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. 2022 Jul 20;1114:21–34. doi: 10.3897/zookeys.1114.85028

Complete mitochondrial genome sequences of Physogyralichtensteini (Milne Edwards & Haime, 1851) and Plerogyrasinuosa (Dana, 1846) (Scleractinia, Plerogyridae): characterisation and phylogenetic analysis

Peng Tian 1, Zhiyu Jia 1, Bingbing Cao 1, Wei Wang 1, Jiaguang Xiao 1, Wentao Niu 1,✉
PMCID: PMC9848633  PMID: 36761708

Abstract

In this study, the whole mitochondrial genomes of Physogyralichtensteini and Plerogyrasinuosa have been sequenced for the first time. The length of their assembled mitogenome sequences were 17,286 bp and 17,586 bp, respectively, both including 13 protein-coding genes, two tRNAs, and two rRNAs. Their mitogenomes offered no distinct structure and their gene order were the same as other typical scleractinians. Based on 13 protein-coding genes, a maximum likelihood phylogenetic analysis showed that Physogyralichtensteini and Plerogyrasinuosa are clustered in the family Plerogyridae, which belongs to the “Robust” clade. The 13 tandem mitogenome PCG sequences used in this research can provide important molecular information to clarify the evolutionary relationships amongst stony corals, especially at the family level. On the other hand, more advanced markers and more species need to be used in the future to confirm the evolutionary relationships of all the scleractinians.

Keywords: Evolutionary relationships, mitogenome data, Plerogyridae, “Robust” clade

Introduction

The order Scleractinia (Cnidaria, Anthozoa), including numerous reef-building coral species, is important as the constructors of coral reefs as an ecosystem. The mitogenome data of cnidarians contain important phylogenetic information for understanding their evolutionary history (Kayal et al. 2013). Single- or multiple-gene analysis of mitochondrial genes have already been used to infer phylogenetic relationships amongst scleractinians (Kitahara et al. 2016; Arrigoni et al. 2020).

In Scleractinia, three main clades have been defined based on molecular analyses, “Complex”, “Robust”, and “Basal” (Romano and Palumbi 1996; Kitahara et al. 2010; Stolarski et al. 2011). Plerogyridae Rowlett, 2020 is a small family of the “Robust” clade of corals containing four genera (Plerogyra Milne Edwards & Haime, 1848, Physogyra Quelch, 1884, Blastomussa Wells, 1968, and Nemenzophyllia Hodgson & Ross, 1982) (see Hoeksema and Cairns 2022), all from the Indo-West Pacific. Previously, the genera Plerogyra and Physogyra were placed in the Euphylliidae of the “Complex” group (Fukami et al. 2008), the family Plesiastreidae of the the “Robust” group (Dai and Horng 2009), and in Scleractinia incertae sedis (Budd et al. 2012; Benzoni et al. 2014; Waheed et al. 2015), but recently Rowlett (2020) placed them in the family Plerogyridae. Physogyra has one recently accepted species and four uncertain species, whereas Plerogyra has seven accepted species (Hoeksema and Cairns 2022). Through molecular analyses of two mitochondrial genes, Fukami et al. (2008) found that Plerogyra and Physogyra do not belong to the “Complex” clade of Scleractinia but to the “Robust” clade. Morphologically, plerogyrid species are characterised by mantle vesicles that are diurnally visible when the tentacles are partially retracted (Benzoni et al. 2014).

Physogyralichtensteini (Milne Edwards & Haime, 1851) and Plerogyrasinuosa (Dana, 1846) are covered by round to irregularly bifurcating vesicles during the day and active, open polyps at night (Veron 2000; Benzoni et al. 2014). Physogyralichtensteini is common in lagoons and reef slopes to deeper than 38 m (De Palmas et al. 2021). Colonies of Physogyralichtensteini are generally massive. They are meandroid, with short, widely separated valleys interconnected with a light, blistery coenosteum. Septa are large, solid, smooth-edged, exsert, and widely spaced. Walls are solid. Columellae are absent. Tentacles are extended only at night. The septal vesicles of Physogyra are considerably smaller and more numerous when compared to the closely related Plerogyra. The colour of Physogyralichtensteini is pale grey or sometimes dull green (Veron 2000), while in Plerogyrasinuosa, the colonies are flabello-meandroid with valleys somewhat connected by a light, blistery coenosteum. Living parts of colonies are sometimes separated by dead basal parts. Vesicles are the size of grapes and usually have the shape of grapes but may be tubular, bifurcated, or irregular, depending primarily upon the state of inflation. The colour of Plerogyrasinuosa is cream or bluish grey. Plerogyrasinuosa is a prominent species and reasonably common in protected reefs, and it is easily recognised by its bubbly appearance (Veron 2000; Rowlett 2020).

In this research, the complete mitochondrial genomes of Physogyralichtensteini and Plerogyrasinuosa are sequenced and their genome structures are analysed for the first time. The phylogenetic analyses of these two species, based on 13 protein coding genes (PCGs) of the mitogenome, in combination with another 42 species of other genera of Scleractinia and two species of Corallimorphidae Hertwig 1882 (order Corallimorpharia) as outgroups, because they are closely related to Scleractinia in evolutionary terms. This helps determine their phylogenetic status and facilitate further study on stony coral evolutionary and phylogenetic relationships.

Materials and methods

Sample collection and genomic DNA extraction

Samples of Physogyralichtensteini (Fig. 1A, C) and Plerogyrasinuosa (Fig. 1B, D) were obtained in 2019 from a coral mariculture company in China, which originally obtained mother stock from Negeri Sabah of Malaysia. Their specimens were maintained in our Coral Sample Repository with the codes 20191207-J2 (Physogyralichtensteini) and 20191207-Y1 (Plerogyrasinuosa). Total genomic DNA was extracted using the DNeasy Blood and Tissue Kit (Qiagen, Shanghai, China). Electrophoresis with 1% agarose gel was used to measure the integrity of their genomic DNA, and a NanoDrop 2000 spectrophotometer (Thermo Fisher Scientific, MA, USA) was used to measure their genomic DNA concentration.

Figure 1.

Figure 1.

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Scleractinian corals used in this study A, CPhysogyralichtensteiniB, DPlerogyrasinuosaA, B live animals C, D skeletons.

Mitogenome sequencing, annotation, and analyses

In this study, two methods were used to obtain the mitogenomes of Physogyralichtensteini and Plerogyrasinuosa, respectively. The complete mitogenome of Plerogyrasinuosa was obtained through a PCR approach using the primer pairs designed by Lin et al. (2011). The complete mitogenome of Physogyralichtensteini was obtained from high-throughput sequencing with a HiSeqX Ten platform (Illumina, San Diego, CA, USA) with a paired-end 150 bp approach according to Tian et al. (2021), and a total of 102,074 of 116,026,504 raw reads (approximately 0.09%) were de novo assembled to produce a single, circular form of the complete mitogenome with an average coverage of 892 X. The circularised contig of these two species were then submitted to the MITOS WebServer (Bernt et al. 2013; http://mitos.bioinf.uni-leipzig.de/index.py) for preliminary mitochondrial genome annotation. We identified and annotated their 13 PCGs and two rRNA genes by alignments of homologous mitogenomes from other scleractinians that had been recovered through BLAST searches in NCBI, and we also validated the tRNA genes using ARWEN (Laslett and Canbäck 2008). The genome structures were mapped using the online CGView Server (Stothard and Wishart 2005; https://proksee.ca/). Base composition, nucleotide frequencies, and codon usage were obtained through MEGA7 (Kumar et al. 2016). The skewing of the nucleotide composition was measured in terms of AT skews and GC skews according to the following formulae: AT skew = (A – T) / (A + T) and GC skew = (G – C) / (G + C) (Perna and Kocher 1995). The mitogenome sequences of Physogyralichtensteini and Plerogyrasinuosa are available in GenBank under accession numbers MW970409 and MW936598.

Phylogenetic analyses

The phylogenetic positions of Physogyralichtensteini and Plerogyrasinuosa were inferred using 13 tandem mitogenome PCG sequences (ND5 + ND1 + Cytb + ND2 + ND6 + ATP6 + ND4 + COIII + COII + ND4L + ND3 + ATP8 + COI) (Tian et al. 2021) together with another 42 species of other genera of Scleractinia and two species belonging to two genera of Corallimorpharia that we obtained from GenBank (Table 1). We used MEGA 7 to select the best-fitting model based on the Akaike Information Criterion (AIC) and then constructed a maximum likelihood (ML) tree with 500 bootstrap replicates.

Table 1.

Representative species of Scleractinia included in this study.

Species Family Mitogenome length (bp) GenBank accession number
1 Physogyralichtensteini Plerogyridae 17,286 MW970409
2 Plerogyrasinuosa Plerogyridae 17,586 MW936598
3 Acroporahorrida Acroporidae 18,480 NC_022825
4 Alveoporajaponica Acroporidae 18,144 MG851913
5 Astreoporaexplanata Acroporidae 18,106 KJ634269
6 Isoporapalifera Acroporidae 18,725 KJ634270
7 Montiporacactus Acroporidae 17,887 NC_006902
8 Agariciafragilis Agariciidae 18,667 KM051016
9 Agariciahumilis Agariciidae 18,735 NC_008160
10 Pavonaclavus Agariciidae 18,315 NC_008165
11 Pavonadecussata Agariciidae 18,378 KP231535
12 Desmophyllumpertusum Caryophylliidae 16,150 FR821799
13 Solenosmiliavariabilis Caryophylliidae 15,968 KM609293
14 Dendrophylliaarbuscula Dendrophylliidae 19,069 KR824937
15 Tubastraeacoccinea Dendrophylliidae 19,094 KX024566
16 Duncanopsammiapeltata Dendrophylliidae 18,966 NC_024671
17 Fimbriaphylliaancora Euphylliidae 18,875 NC_015641
18 Galaxeafascicularis Euphylliidae 18,751 NC_029696
19 Colpophyllianatans Faviidae 16,906 NC_008162
20 Mussaangulosa Faviidae 17,245 DQ643834
21 Fungiacyathusstephanus Fungiacyathidae 19,381 JF825138
22 Gardineriahawaiiensis Gardineriidae 19,430 MT376619
23 Echinophylliaaspera Lobophylliidae 17,697 MG792550
24 Dipsastraearotumana Merulinidae 16,466 MH119077
25 Hydnophoraexesa Merulinidae 17,790 MH086217
26 Orbicellafaveolata Merulinidae 16,138 AP008978
27 Platygyracarnosa Merulinidae 16,463 JX911333
28 Letepsammiaformosissima Micrabaciidae 19,048 MT705247
29 Letepsammiasuperstes Micrabaciidae 19,073 MT706035
30 Rhombopsammianiphada Micrabaciidae 19,542 MT706034
31 Madreporaoculata Oculinidae 15,841 JX236041
32 Plesiastreaversipora Plesiastreidae 15,320 MH025639
33 Pocilloporaeydouxi Pocilloporidae 17,422 EF526303
34 Seriatoporahystrix Pocilloporidae 17,059 EF633600.2
35 Madracismirabilis Pocilloporidae 16,951 NC_011160
36 Stylophorapistillata Pocilloporidae 17,177 NC_011162
37 Gonioporacolumna Poritidae 18,766 JF825141
38 Poritesfontanesii Poritidae 18,658 NC_037434
39 Poriteslobata Poritidae 18,647 KU572435
40 Poritesrus Poritidae 18,647 NC_027526
41 Psammocoraprofundacella Psammocoridae 16,274 MT576637
42 Astrangiapoculata Astrangiidae 14,853 NC_008161
43 Pseudosiderastreatayami Siderastreidae 19,475 KP260633
44 Siderastrearadians Siderastreidae 19,387 NC_008167
45 Corallimorphusprofundus Corallimorphidae 20,488 KP938440
46 Corynactiscalifornica Corallimorphidae 20,715 NC_027102
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Results and discussion

Characteristics and composition of mitogenome

The mitochondrial genome sizes of Physogyralichtensteini and Plerogyrasinuosa are 17,286 bp and 17,586 bp, respectively, both including 13 PCGs, two tRNA (tRNAMet, tRNATrp), and two rRNA genes (Tables 2, 3; Fig. 2). Their mitogenomes offer no distinct structure and their gene orders are same as other typical scleractinians (Lin et al. 2012). All genes are encoded on the H-strand. The base composition of the complete mitogenome is 24.75% A, 13.32% C, 21.75% G, and 40.17% T for Physogyralichtensteini, and 24.87% A, 13.16% C, 22.01% G, and 39.96% T for Plerogyrasinuosa. Both species show a higher AT content than GC content (Fig. 3; Table 4).

Table 2.

Organisation of the mitochondrial genome of Physogyralichtensteini.

Gene Position Length (bp) Anticodon Codon Intergenic nucleotides* Strand†
From To Start Stop
tRNAMet 1 72 72 CAU 1228 H
16S rRNA 270 1967 1698 197 H
ND5 5’ 1998 2708 711 ATG 30 H
ND1 2817 3764 948 ATG TAG 108 H
Cytb 3767 4906 1140 ATG TAA 2 H
ND2 5124 6218 1095 TTA TAA 217 H
ND6 6219 6779 561 ATG TAA 0 H
ATP6 6779 7453 675 ATG TAA −1 H
ND4 7453 8892 1440 ATG TAG −1 H
12S rRNA 8890 9800 911 −3 H
COIII 9794 10573 780 ATG TAA −7 H
COII 10576 11283 708 ATG TAG 2 H
ND4L 11265 11564 300 ATG TAG −19 H
ND3 11567 11908 342 GTG TAA 2 H
ND5 3’ 11996 13099 1104 TAG 87 H
tRNATrp 13098 13166 69 UCA −2 H
ATP8 13170 13367 198 ATG TAA 3 H
COI 5’ 13385 14095 711 ATT 17 H
COI 3’ 15173 16057 885 TAG 1077 H
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*Data are number of nucleotides between the given gene and its previous gene; negative numbers indicate overlapping nucleotides. †H indicates that the genes transcribed on the heavy strand.

Table 3.

Organisation of the mitochondrial genome of Plerogyrasinuosa.

Gene Position Length (bp) Anticodon Codon Intergenic nucleotides* Strand†
From To Start Stop
tRNAMet 1 72 72 CAU 1581 H
16S rRNA 272 1969 1698 199 H
ND5 5’ 2000 2710 711 ATG 30 H
ND1 2819 3766 948 ATG TAG 108 H
Cytb 3769 4908 1140 ATG TAA 2 H
ND2 5125 6219 1095 TTA TAA 216 H
ND6 6220 6780 561 ATG TAA 0 H
ATP6 6780 7454 675 ATG TAA −1 H
ND4 7451 8893 1443 ATG TAG −4 H
12S rRNA 8891 9797 907 −3 H
COIII 9795 10574 780 ATG TAA −3 H
COII 10577 11284 708 ATG TAG 2 H
ND4L 11266 11565 300 ATG TAG −19 H
ND3 11568 11909 342 GTG TAA 2 H
ND5 3’ 11997 13100 1104 TAG 87 H
tRNATrp 13099 13167 69 UCA −2 H
ATP8 13171 13368 198 ATG TAA 3 H
COI 5’ 13368 14270 903 ATG −1 H
COI 3’ 15336 16004 669 TAA 1065 H
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*Data are number of nucleotides between the given gene and its previous gene; negative numbers indicate overlapping nucleotides. †H indicates that the genes transcribed on the heavy strand.

Figure 2.

Figure 2.

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The mitogenome order and positions of Physogyralichtensteini and Plerogyrasinuosa. COI, COII, and COIII refer to the cytochrome oxidase subunits, Cyt b refers to cytochrome b, and ND1–ND6 refers to NADH dehydrogenase components. All the genes are encoded on the H-strand.

Figure 3.

Figure 3.

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Codon usage bias in the different regions of the mitogenomes of Physogyralichtensteini and Plerogyrasinuosa.

Table 4.

Nucleotide composition in different regions of mitogenomes of Physogyralichtensteini (P.l.) and Plerogyrasinuosa (P.s.).

Gene/Region T (%) C (%) A (%) G (%) A+T (%) Size (bp)
P.l. P.s. P.l. P.s. P.l. P.s. P.l. P.s. P.l. P.s. P.l. P.s.
ND5 46.56 46.61 12.07 12.01 21.71 21.76 19.67 19.61 68.27 68.37 1815 1815
ND1 43.35 43.46 14.14 14.03 19.20 19.09 23.31 23.42 62.55 62.55 948 948
Cytb 44.91 44.82 13.68 13.68 20.88 20.88 20.53 20.61 65.79 65.70 1140 1140
ND2 47.31 47.31 12.79 12.60 20.00 20.09 19.91 20.00 67.31 67.40 1095 1095
ND6 44.56 44.56 13.37 13.55 22.28 22.28 19.79 19.61 66.84 66.84 561 561
ATP6 46.81 46.37 13.19 13.33 22.22 22.22 17.78 18.07 69.03 68.59 675 675
ND4 45.35 45.56 13.54 13.47 19.86 19.86 21.25 21.11 65.21 65.42 1440 1443
COIII 42.69 42.69 15.38 15.51 19.74 19.62 22.18 22.18 62.43 62.31 780 780
COII 39.69 39.55 13.28 13.28 24.01 23.87 23.02 23.31 63.70 63.42 708 708
ND4L 44.33 44.33 12.00 12.00 24.67 24.67 19.00 19.00 69.00 69.00 300 300
ND3 47.08 46.78 9.94 9.94 17.84 17.84 25.15 25.44 64.92 64.62 342 342
ATP8 43.43 43.43 12.12 12.12 29.29 29.29 15.15 15.15 72.72 72.72 198 198
COI 40.41 39.31 15.10 15.78 22.12 22.20 22.37 22.71 62.53 61.51 1596 1572
PCGs 44.35 44.20 13.42 13.50 21.25 21.25 20.98 21.06 65.60 65.45 11598 11574
1st 35.59 35.56 13.63 13.69 21.99 21.90 28.79 28.85 57.58 57.47 3866 3858
2nd 47.31 47.15 18.65 18.61 17.93 18.01 16.11 16.23 65.24 65.16 3866 3858
3rd 50.16 49.90 7.99 8.19 23.82 23.82 18.03 18.09 73.98 73.72 3866 3858
tRNA 24.82 24.82 23.40 23.40 27.66 27.66 24.11 24.11 52.48 52.48 141 141
rRNA 31.70 31.67 12.50 12.48 35.19 35.12 20.62 20.73 66.89 66.79 2609 2605
Overall 40.17 39.96 13.32 13.16 24.75 24.87 21.75 22.01 64.92 64.83 17286 17586
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Protein-coding genes

The lengths of all 13 protein-coding genes (PCGs) are 11,598 bp and 11,574 bp for Physogyralichtensteini and Plerogyrasinuosa, respectively. In both species, the ND5 gene and COI gene have intron insertions, and the start and stop codon of all 13 PCGs are exactly the same except for the COI gene. Their shortest gene is in both ATP8, and their longest gene is ND5 (Tables 2, 3). According to the AT-skew and GC-skew analyses (Fig. 4), both PCGs of Physogyralichtensteini and Plerogyrasinuosa show a stronger nucleotide asymmetry, with AT skew higher than GC skew. Amongst L, F, V, G, and S in Physogyralichtensteini and Plerogyrasinuosa, codon use frequency was higher, accounting for 53.5% and 53.4%, respectively. In their 20 amino acids, the majority are non-polar amino acids, and a minority are polarity-charged amino acids (Fig. 5).

Figure 4.

Figure 4.

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The PCG AT skew and GC skew of the mitochondrial genomes of Physogyralichtensteini and Plerogyrasinuosa.

Figure 5.

Figure 5.

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The PCG codon use frequency of the mitochondrial genomes of Physogyralichtensteini and Plerogyrasinuosa.

rRNA and tRNA genes

The encoding genes 12S and 16S rRNA in Physogyralichtensteini are 911 bp and 1,698 bp in size, and in Plerogyrasinuosa they are 907 bp and 1,698 bp in size. The base composition of rRNA in Physogyralichtensteini was 35.19% A, 12.5% C, 20.62% G, and 31.7% T, and in Plerogyrasinuosa it was 35.12% A, 12.48% C, 20.73% G, and 31.67% T. The two tRNA encoding genes, tRNAMet (72 bp) and tRNATrp (69 bp), are exactly the same in Physogyralichtensteini and Plerogyrasinuosa (Tables 2, 3). They are folded into the classic cloverleaf structure which includes an amino acid accept arm, DHU loop, anticodon loop, and TψC loop (Fig. 6).

Figure 6.

Figure 6.

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Putative secondary structures of two tRNAs in Physogyralichtensteini and Plerogyrasinuosa.

Phylogenetic analyses

There are three distinct clades of Scleractinia in our ML tree, including “Complex”, “Robust”, and “Basal” clade. The ML topology tree of all the 47 species shows that Physogyralichtensteini and Plerogyrasinuosa are clustered in family Plerogyridae which belong to the “Robust” clade with high bootstrap support (Fig. 7). Our finding is consistent with the results of Fukami et al. (2008) who placed Plerogyra and Physogyra in the “Robust” clade. From the ML tree we also find that Physogyralichtensteini and Plerogyrasinuosa are a sister group with Astrangiapoculata, which belongs to the family Astrangiidae Milne Edwards & Haime, 1857. Our MT tree of the Plerogyridae shows the same classification as used by Rowlett (2020). Single- or multi-gene analyses of mitochondrial genes have already been used to infer phylogenetic relationships amongst scleractinians (Kitahara et al. 2016; Arrigoni et al. 2020). The 13 tandem mitogenome PCG sequences we used in this research can provide important molecular information to understand the evolutionary relationships amongst stony corals, especially at the family level. As fewer than a tenth of stony coral species have been sequenced at this time, more mitogenomes of other scleractinians are necessary before accurate family-level evolutionary relationships can be reconstructed. In the future, more advanced markers and more species should be used to confirm the evolutionary relationships among all scleractinians.

Figure 7.

Figure 7.

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Inferred phylogenetic relationships based on a maximum-likelihood analysis of concatenated nucleotide sequences of 13 mitochondrial PCGs. Numbers on branches are bootstrap percentages.

Conclusions

The complete mitochondrial genomes of Physogyralichtensteini and Plerogyrasinuosa were sequenced for the first time. Their mitogenomes show a similar gene order and composition with other typical Scleractinia. Our phylogenetic analysis of Physogyralichtensteini and Plerogyrasinuosa, based on their 13 tandem mitochondrial protein-coding genes and including another 42 species of Scleractinia and two species of Corallimorpharia, help us to understand the evolutionary relationships amongst stony corals and facilitate further studies on stony coral evolutionary and phylogenetic relationships.

Acknowledgements

This study was funded by the National Natural Science Foundation of China (grant number 42106143; 42006128); National key research and development program(021YFC3100503); the Scientific Research Foundation of Third Institute of Oceanography, Ministry of Natural Resources (grant number 2022024; 2020006); and Nansha Islands Coral Reef Ecosystem National Observation and Research Station (NSICR). PT and WN conceived, designed, and performed the study. ZJ, BC, JX, and WW processed and analysed the data. All authors contributed to the preparation of the manuscript.

Citation

Tian P, Jia Z, Cao B, Wang W, Xiao J, Niu W (2022) Complete mitochondrial genome sequences of Physogyra lichtensteini (Milne Edwards & Haime, 1851) and Plerogyra sinuosa (Dana, 1846) (Scleractinia, Plerogyridae): characterisation and phylogenetic analysis. ZooKeys 1114: 21–34. https://doi.org/10.3897/zookeys.1114.85028

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