http://informahealthcare.com/mdn ISSN: 1940-1736 (print), 1940-1744 (electronic) Mitochondrial DNA, Early Online: 1–2 ! 2014 Informa UK Ltd. DOI: 10.3109/19401736.2014.908359
MITOGENOME ANNOUNCEMENT
Mitochondrial genome architecture of the giant red sea urchin Mesocentrotus franciscanus (Strongylocentrotidae, Echinoida) Juan Diego Gaita´n-Espitia1 and Gretchen E. Hofmann2 Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile and 2Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA, USA
Mitochondrial DNA Downloaded from informahealthcare.com by University of Sydney on 09/04/14 For personal use only.
1
Abstract
Keywords
The complete mitochondrial genome of the Californian giant red sea urchin Mesocentrotus franciscanus has been determined. It has a length of 15,650 bp and contains the same 37 genes found in other metazoans (13 protein-coding genes, 22 tRNA genes, and two rRNA genes). Only five tRNA genes and the Nad6 gene are coded on the minus strand. There were 14 identified small intergene regions (2 to 24 bp) and a large non-coding region (125 bp) located between the tRNA-T and tRNA-P. The overall base composition of this genome is 29.8% A, 27.6% T, 29.7% C, and 17.5% G, with a slight A + T bias of 59.4%. The most frequent start codon is ATG (11 genes) whereas TAA is the most frequent stop codon (10 genes). Overall, gene arrangement pattern, gene content and genome organization is similar to other echinoids
Mesocentrotus franciscanus, mitogenome, sea urchins, Strongylocentrotidae
Echinoids (sea urchins and sand dollars) are one of the most abundant and ecologically successful groups of marine invertebrates on earth (Lawrence, 2013). This group is part of an ancient and highly derived deuterostome phylum (i.e. Echinodermata) characterized by the presence of a water vascular system and a form of calcium carbonate endoskeleton called stereom (Amemiya et al., 2005; Shen et al., 2009). Within echinoids, sea urchins of the family Strongylocentrotidae have been widely used as biological models for evolutionary biology studies (Kober & Bernardi, 2013; Lee, 2003). Molecular phylogenies based on mitochondrial genes have identified two main clades within Strongylocentrotidae, one consisting of members of Strongylocentrotus and Hemicentrotus and the other consisting of Mesocentrotus and Pseudocentrotus (Biermann et al., 2003; Kober & Bernardi, 2013). Here, using next-generation sequencing (NGS) technology, we describe the complete mitochondrial genome of the Californian giant red sea urchin Mesocentrotus franciscanus. This sea urchin was previously considered as a member of the
History Received 7 March 2014 Revised 15 March 2014 Accepted 22 March 2014 Published online 14 April 2014
genus Strongylocentrotus, but recent genetic and morphological evidences allowed the transference of S. franciscanus to M. franciscanus (Biermann et al., 2003; Kober & Bernardi, 2013; Lawrence, 2013). Mitochondrial genes were identified using DOGMA (Wyman et al., 2004). Transfer RNA genes were located and folded by their proposed cloverleaf to confirm their secondary structures (supporting information is available upon request from the authors) using the tRNAscan-SE v.1.21 (Santa Cruz, CA) (Schattner et al., 2005). The complete mitochondrial genome of M. franciscanus (GenBank accession number KJ526170) is a circular molecule with 15,650 bp in length and contains the same 37 genes found in other metazoans: 13 protein-coding genes, 22 transfer RNA genes, and two ribosomal RNA genes (Table 1). From these 37 genes, only six are coded on the minus strand: tRNA-Q, tRNA-A, tRNA-V, tRNA-D, tRNA-S1, and Nad6 (Table 1). This mitochondrial genome includes 14 small size-variable intergene regions ranging from 2 to 24 bp, and a large non-coding region (125 bp) located between the tRNA-T and tRNA-P (Table 1), that contains the
Table 1. Mitochondrial genome content and general features of the red sea urchin Mesocentrotus franciscanus. Name
Direction
Length (bp)
tRNA-Phe F 12s rRNA tRNA-Glu E tRNA-Thr T POR
Forward Forward Forward Forward
73 896 69 74 125
Min
Max
1 74 970 1043 1116
73 970 1038 1115 1240
Start codon
Stop codon
Anti-codon
AT %
35–37 GAA 1000–1002 TTC 1077–1079 TGT
58.0 52.1 53.6 (continued )
Correspondence: Juan Diego Gaita´n-Espitia, Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Casilla 567, Valdivia, Chile. Tel: [++56] (63) 221704. Fax: [++56] (63) 221344. E-mail: [email protected]
2
J. D. Gaita´n-Espitia & G. E. Hofmann
Mitochondrial DNA, Early Online: 1–2
Mitochondrial DNA Downloaded from informahealthcare.com by University of Sydney on 09/04/14 For personal use only.
Table 1. Continued
Name
Direction
Length (bp)
Min
Max
tRNA-Pro P tRNA-Gln Q tRNA-Asn N tRNA-Leu L1 tRNA-Ala A tRNA-Trp W tRNA-Cys C tRNA-Val V tRNA-Met M tRNA-Asp D tRNA-Tyr Y tRNA-Gly G tRNA-Leu L2 Nad 1 tRNA-Ile I Nad 2 16s rRNA Cox 1 tRNA-Arg R Nad4L Cox 2 tRNA-Lys K Atp 8 Atp 6 Cox 3 tRNA-Ser S1 Nad 3 Nad 4 tRNA-His H tRNA-Ser S2 Nad 5 Nad 6 Cytb
Forward Reverse Forward Forward Reverse Forward Forward Reverse Forward Reverse Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Reverse Forward Forward Forward Forward Forward Reverse Forward
73 72 72 72 71 69 68 70 76 70 74 71 74 972 73 1059 1542 1554 69 294 690 71 165 684 783 70 351 1389 69 68 1854 489 1143
1240 1313 1394 1466 1607 1610 1679 1815 1839 1983 1990 2066 2135 2210 3183 3255 4314 5851 7414 7484 7777 8471 8542 8703 9390 10,241 10,258 10,623 12,002 12,072 12,140 14,482 14,507
1312 1384 1465 1537 1537 1678 1746 1746 1914 1914 2063 2136 2208 3181 3255 4313 5854 7404 7482 7777 8466 8541 8706 9386 10,172 10,172 10,608 12,011 12,070 12,139 13,993 13,994 15,649
putative origin for mitochondrial DNA replication (POR). There were identified small gene overlaps at 18 gene borders, the largest has a length of 10 nucleotides and is located between Nad4 and tRNA-H. The overall base composition of this genome was: 29.8% A, 27.6% T, 29.7% C, and 17.5% G, with a slight A + T bias of 59.4%. All protein-coding genes used ATG as the start codon except for the genes Atp6 and Atp8 that used GTA and GTG respectively. Ten genes used TAA as stop codon while three used TAG (Table 1). In general, the mitochondrial genome of M. franciscanus retains the same gene arrangement pattern, gene content and genome organization of other echinoids (Perseke et al., 2008, 2010), which is consistent with the highly conserved genome architecture of Echinoidea (Perseke et al., 2008).
Declaration of interest JDGE was supported by a postdoctoral fellowship from Fondo Nacional de Desarrollo Cientı´fico y Tecnolo´gico (FONDECYT-Postdoctoral grant N 3130381). The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the manuscript.
References Amemiya CT, Miyake T, Rast JP. (2005). Echinoderms. Curr Biol 15: R944–6.
Start codon
Stop codon
Anti-codon 1272–1274 1351–1349 1426–1428 1499–1501 1575–1573 1640–1642 1709–1711 1784–1782 1873–1875 1952–1950 2023–2025 2095–2097 2168–2170
ATG
AT %
TGG TTG GTT TAG TGC TCA GCA TAC CAT GTC GTA TCC TAA
TAA
59.6 3215–3217 GAT
ATG
TAG
ATG
TAA
ATC ATG
TAA TAA
GTG GTA ATG
TAA TAA TAA
ATG ATG
TAA TAG
60.9 61.8 56.5 7444–7446 TCG 60.5 57.7 8502–8504 CTT 64.2 61.5 57.1 10,210–10,208 TGA 55.6 58.8 12,032–12,035 GTG 12,105–12,107 CCA
ATG ATG ATG
TAA TAG TAA
60.3 60.7 58.6
Biermann CH, Kessing BD, Palumbi SR. (2003). Phylogeny and development of marine model species: Strongylocentrotid sea urchins. Evol Dev 5:360–71. Kober KM, Bernardi G. (2013). Phylogenomics of strongylocentrotid sea urchins. BMC Evol Biol 13:88. Lawrence JM. (2013). Sea urchins: Biology and ecology. Amsterdam: Elsevier. Lee Y-H. (2003). Molecular phylogenies and divergence times of sea urchin species of Strongylocentrotidae, Echinoida. Mol Biol Evol 20: 1211–21. Perseke M, Bernhard D, Fritzsch G, Bru¨mmer F, Stadler PF, Schlegel M. (2010). Mitochondrial genome evolution in Ophiuroidea, Echinoidea, and Holothuroidea: Insights in phylogenetic relationships of Echinodermata. Mol Phylogenet Evol 56:201–11. Perseke M, Fritzsch G, Ramsch K, Bernt M, Merkle D, Middendorf M, Bernhard D, et al. (2008). Evolution of mitochondrial gene orders in echinoderms. Mol Phylogenet Evol 47:855–64. Schattner P, Brooks AN, Lowe TM. (2005). The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–9. Shen X, Tian M, Liu Z, Cheng H, Tan J, Meng X, Ren J. (2009). Complete mitochondrial genome of the sea cucumber Apostichopus japonicus (Echinodermata: Holothuroidea): The first representative from the subclass Aspidochirotacea with the echinoderm ground pattern. Gene 439:79–86. Wyman SK, Jansen RK, Boore JL. (2004). Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252–5.
MITOGENOME ANNOUNCEMENT
Mitochondrial genome architecture of the giant red sea urchin Mesocentrotus franciscanus (Strongylocentrotidae, Echinoida) Juan Diego Gaita´n-Espitia1 and Gretchen E. Hofmann2 Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile and 2Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA, USA
Mitochondrial DNA Downloaded from informahealthcare.com by University of Sydney on 09/04/14 For personal use only.
1
Abstract
Keywords
The complete mitochondrial genome of the Californian giant red sea urchin Mesocentrotus franciscanus has been determined. It has a length of 15,650 bp and contains the same 37 genes found in other metazoans (13 protein-coding genes, 22 tRNA genes, and two rRNA genes). Only five tRNA genes and the Nad6 gene are coded on the minus strand. There were 14 identified small intergene regions (2 to 24 bp) and a large non-coding region (125 bp) located between the tRNA-T and tRNA-P. The overall base composition of this genome is 29.8% A, 27.6% T, 29.7% C, and 17.5% G, with a slight A + T bias of 59.4%. The most frequent start codon is ATG (11 genes) whereas TAA is the most frequent stop codon (10 genes). Overall, gene arrangement pattern, gene content and genome organization is similar to other echinoids
Mesocentrotus franciscanus, mitogenome, sea urchins, Strongylocentrotidae
Echinoids (sea urchins and sand dollars) are one of the most abundant and ecologically successful groups of marine invertebrates on earth (Lawrence, 2013). This group is part of an ancient and highly derived deuterostome phylum (i.e. Echinodermata) characterized by the presence of a water vascular system and a form of calcium carbonate endoskeleton called stereom (Amemiya et al., 2005; Shen et al., 2009). Within echinoids, sea urchins of the family Strongylocentrotidae have been widely used as biological models for evolutionary biology studies (Kober & Bernardi, 2013; Lee, 2003). Molecular phylogenies based on mitochondrial genes have identified two main clades within Strongylocentrotidae, one consisting of members of Strongylocentrotus and Hemicentrotus and the other consisting of Mesocentrotus and Pseudocentrotus (Biermann et al., 2003; Kober & Bernardi, 2013). Here, using next-generation sequencing (NGS) technology, we describe the complete mitochondrial genome of the Californian giant red sea urchin Mesocentrotus franciscanus. This sea urchin was previously considered as a member of the
History Received 7 March 2014 Revised 15 March 2014 Accepted 22 March 2014 Published online 14 April 2014
genus Strongylocentrotus, but recent genetic and morphological evidences allowed the transference of S. franciscanus to M. franciscanus (Biermann et al., 2003; Kober & Bernardi, 2013; Lawrence, 2013). Mitochondrial genes were identified using DOGMA (Wyman et al., 2004). Transfer RNA genes were located and folded by their proposed cloverleaf to confirm their secondary structures (supporting information is available upon request from the authors) using the tRNAscan-SE v.1.21 (Santa Cruz, CA) (Schattner et al., 2005). The complete mitochondrial genome of M. franciscanus (GenBank accession number KJ526170) is a circular molecule with 15,650 bp in length and contains the same 37 genes found in other metazoans: 13 protein-coding genes, 22 transfer RNA genes, and two ribosomal RNA genes (Table 1). From these 37 genes, only six are coded on the minus strand: tRNA-Q, tRNA-A, tRNA-V, tRNA-D, tRNA-S1, and Nad6 (Table 1). This mitochondrial genome includes 14 small size-variable intergene regions ranging from 2 to 24 bp, and a large non-coding region (125 bp) located between the tRNA-T and tRNA-P (Table 1), that contains the
Table 1. Mitochondrial genome content and general features of the red sea urchin Mesocentrotus franciscanus. Name
Direction
Length (bp)
tRNA-Phe F 12s rRNA tRNA-Glu E tRNA-Thr T POR
Forward Forward Forward Forward
73 896 69 74 125
Min
Max
1 74 970 1043 1116
73 970 1038 1115 1240
Start codon
Stop codon
Anti-codon
AT %
35–37 GAA 1000–1002 TTC 1077–1079 TGT
58.0 52.1 53.6 (continued )
Correspondence: Juan Diego Gaita´n-Espitia, Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Casilla 567, Valdivia, Chile. Tel: [++56] (63) 221704. Fax: [++56] (63) 221344. E-mail: [email protected]
2
J. D. Gaita´n-Espitia & G. E. Hofmann
Mitochondrial DNA, Early Online: 1–2
Mitochondrial DNA Downloaded from informahealthcare.com by University of Sydney on 09/04/14 For personal use only.
Table 1. Continued
Name
Direction
Length (bp)
Min
Max
tRNA-Pro P tRNA-Gln Q tRNA-Asn N tRNA-Leu L1 tRNA-Ala A tRNA-Trp W tRNA-Cys C tRNA-Val V tRNA-Met M tRNA-Asp D tRNA-Tyr Y tRNA-Gly G tRNA-Leu L2 Nad 1 tRNA-Ile I Nad 2 16s rRNA Cox 1 tRNA-Arg R Nad4L Cox 2 tRNA-Lys K Atp 8 Atp 6 Cox 3 tRNA-Ser S1 Nad 3 Nad 4 tRNA-His H tRNA-Ser S2 Nad 5 Nad 6 Cytb
Forward Reverse Forward Forward Reverse Forward Forward Reverse Forward Reverse Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Forward Reverse Forward Forward Forward Forward Forward Reverse Forward
73 72 72 72 71 69 68 70 76 70 74 71 74 972 73 1059 1542 1554 69 294 690 71 165 684 783 70 351 1389 69 68 1854 489 1143
1240 1313 1394 1466 1607 1610 1679 1815 1839 1983 1990 2066 2135 2210 3183 3255 4314 5851 7414 7484 7777 8471 8542 8703 9390 10,241 10,258 10,623 12,002 12,072 12,140 14,482 14,507
1312 1384 1465 1537 1537 1678 1746 1746 1914 1914 2063 2136 2208 3181 3255 4313 5854 7404 7482 7777 8466 8541 8706 9386 10,172 10,172 10,608 12,011 12,070 12,139 13,993 13,994 15,649
putative origin for mitochondrial DNA replication (POR). There were identified small gene overlaps at 18 gene borders, the largest has a length of 10 nucleotides and is located between Nad4 and tRNA-H. The overall base composition of this genome was: 29.8% A, 27.6% T, 29.7% C, and 17.5% G, with a slight A + T bias of 59.4%. All protein-coding genes used ATG as the start codon except for the genes Atp6 and Atp8 that used GTA and GTG respectively. Ten genes used TAA as stop codon while three used TAG (Table 1). In general, the mitochondrial genome of M. franciscanus retains the same gene arrangement pattern, gene content and genome organization of other echinoids (Perseke et al., 2008, 2010), which is consistent with the highly conserved genome architecture of Echinoidea (Perseke et al., 2008).
Declaration of interest JDGE was supported by a postdoctoral fellowship from Fondo Nacional de Desarrollo Cientı´fico y Tecnolo´gico (FONDECYT-Postdoctoral grant N 3130381). The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the manuscript.
References Amemiya CT, Miyake T, Rast JP. (2005). Echinoderms. Curr Biol 15: R944–6.
Start codon
Stop codon
Anti-codon 1272–1274 1351–1349 1426–1428 1499–1501 1575–1573 1640–1642 1709–1711 1784–1782 1873–1875 1952–1950 2023–2025 2095–2097 2168–2170
ATG
AT %
TGG TTG GTT TAG TGC TCA GCA TAC CAT GTC GTA TCC TAA
TAA
59.6 3215–3217 GAT
ATG
TAG
ATG
TAA
ATC ATG
TAA TAA
GTG GTA ATG
TAA TAA TAA
ATG ATG
TAA TAG
60.9 61.8 56.5 7444–7446 TCG 60.5 57.7 8502–8504 CTT 64.2 61.5 57.1 10,210–10,208 TGA 55.6 58.8 12,032–12,035 GTG 12,105–12,107 CCA
ATG ATG ATG
TAA TAG TAA
60.3 60.7 58.6
Biermann CH, Kessing BD, Palumbi SR. (2003). Phylogeny and development of marine model species: Strongylocentrotid sea urchins. Evol Dev 5:360–71. Kober KM, Bernardi G. (2013). Phylogenomics of strongylocentrotid sea urchins. BMC Evol Biol 13:88. Lawrence JM. (2013). Sea urchins: Biology and ecology. Amsterdam: Elsevier. Lee Y-H. (2003). Molecular phylogenies and divergence times of sea urchin species of Strongylocentrotidae, Echinoida. Mol Biol Evol 20: 1211–21. Perseke M, Bernhard D, Fritzsch G, Bru¨mmer F, Stadler PF, Schlegel M. (2010). Mitochondrial genome evolution in Ophiuroidea, Echinoidea, and Holothuroidea: Insights in phylogenetic relationships of Echinodermata. Mol Phylogenet Evol 56:201–11. Perseke M, Fritzsch G, Ramsch K, Bernt M, Merkle D, Middendorf M, Bernhard D, et al. (2008). Evolution of mitochondrial gene orders in echinoderms. Mol Phylogenet Evol 47:855–64. Schattner P, Brooks AN, Lowe TM. (2005). The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–9. Shen X, Tian M, Liu Z, Cheng H, Tan J, Meng X, Ren J. (2009). Complete mitochondrial genome of the sea cucumber Apostichopus japonicus (Echinodermata: Holothuroidea): The first representative from the subclass Aspidochirotacea with the echinoderm ground pattern. Gene 439:79–86. Wyman SK, Jansen RK, Boore JL. (2004). Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252–5.
