http://informahealthcare.com/mdn ISSN: 1940-1736 (print), 1940-1744 (electronic) Mitochondrial DNA, Early Online: 1–3 ! 2014 Informa UK Ltd. DOI: 10.3109/19401736.2014.936417

MITOGENOME ANNOUNCEMENT

Complete mitochondrial genome of the brown alga Sargassum fusiforme (Sargassaceae, Phaeophyceae): genome architecture and taxonomic consideration Feng Liu1, Shaojun Pang1, and Minbo Luo2 Mitochondrial DNA Downloaded from informahealthcare.com by University of Washington on 08/22/14 For personal use only.

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Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, P. R. China and 2Key Laboratory of East China Sea and Oceanic Fishery Resources Exploitation and Utilization, Ministry of Agriculture, East China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Shanghai, P.R. China Abstract

Keywords

Sargassum fusiforme (Harvey) Setchell (¼Hizikia fusiformis (Harvey) Okamura) is one of the most important economic seaweeds for mariculture in China. In this study, we present the complete mitochondrial genome of S. fusiforme. The genome is 34,696 bp in length with circular organization, encoding the standard set of three ribosomal RNA genes (rRNA), 25 transfer RNA genes (tRNA), 35 protein-coding genes, and two conserved open reading frames (ORFs). Its total AT content is 62.47%, lower than other brown algae except Pylaiella littoralis. The mitogenome carries 1571 bp of intergenic region constituting 4.53% of the genome, and 13 pairs of overlapping genes with the overlap size from 1 to 90 bp. The phylogenetic analyses based on 35 protein-coding genes reveal that S. fusiforme has a closer evolutionary relationship with Sargassum muticum than Sargassum horneri, indicating Hizikia are not distinct evolutionary entity and should be reduced to synonymy with Sargassum.

Hizikia fusiformis, mitochondrial genome, Phaeophyceae, Sargassaceae, Sargassum fusiforme

Hizikia fusiformis (Harvey) Okamura, currently regarded as a taxonomic synonym of Sargassum fusiforme (Harvey) Setchell (Guiry & Guiry, 2014), grows on lower intertidal and upper subtidal rocks, especially distributed in Pacific Northwest coasts (Hu et al., 2013; Yu et al., 2012). It is one of the most important seaweeds for mariculture in China due to the increasing economic value and market demand (Pang et al., 2005; Zou & Gao, 2010). The genus Hizikia was established by Okamura (1932) according to morphological features, but molecular data inferred from ITS2 nrDNA indicated that H. fusiformis should be assigned to the genus Sargassum (Stiger et al., 2003). Previously, we reported two Sargassum mitogenomes (Liu & Pang, 2014; Liu et al., 2014), and here we determined the complete mitochondrial genome of S. fusiforme/H. fusiformis (sampled from Nanji Island, China), and reassessed its reliable taxonomic status inferred from mitogenome data. The S. fusiforme mitogenome is a circular molecule of 34,696 bp (GenBank accession number KJ946428), which is 90 bp longer than that of Sargassum horneri and 24 bp shorter than Sargassum muticum. The overall AT content of S. fusiforme mitogenome is 62.47%, lower than other reported brown algae from 63.40% in Desmarestia viridis to 67.47% in Undaria pinnatifida except Pylaiella littoralis (62.01%) (Li et al., 2014; Oudot-Le Secq et al., 2001, 2006). This mitogenome carries

Correspondence: Feng Liu, Shaojun Pang, Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, P. R. China. E-mail: liufeng@ qdio.ac.cn (F. Liu); [email protected] (S. Pang)

History Received 10 June 2014 Accepted 15 June 2014 Published online 3 July 2014

1571 bp of intergenic region constituting 4.53% of the genome, and 13 pairs of overlapping genes with the overlap size from 1 to 90 bp. The S. fusiforme mitogenome contains 65 genes, encoding three ribosomal RNA genes (rRNA), 25 transfer RNA genes (tRNA), 35 protein-coding genes, and two conserved open reading frames (ORFs) (Table 1). The heavy strand encodes 59 genes while the light strand has 6 genes. All protein-coding genes exhibit a methionine (ATG) start codon, and all three typical stop codons are used with a preference of 67.57% for TAA, compared with 21.62% for TAG and 10.81% for TGA. Three Sargassum mitochondrial genomes, i.e. S. fusiforme, S. muticum and S. horneri designated in subgenus Bactrophycus (Mattio & Payri, 2011), turn out to have identical genome architecture, gene content and transcriptional direction, suggesting their close evolutionary relationships. The mitogenome of S. fusiforme has an overall nucleotide sequence identity of 89.1% with S. muticum, which is higher than 87.6% between S. fusiforme and S. horneri and 87.9% between S. muticum and S. horneri, respectively. The nucleotide and/or amino acid sequence identities of 65 genes of three Sargassum species are summarized in Table 1. The phylogenetic analyses based on 35 protein-coding genes show that S. fusiforme firstly groups with S. muticum with high bootstrap support values (ML/NJ, 100%), and then these two species form a monophyletic group together with S. horneri, indicating that S. fusiforme has a closer evolutionary relationship with S. muticum than S. horneri. Present results obtained in genomic level, combined with earlier findings from molecular data, provide strong evidences that Hizikia is not distinct evolutionary entity and should be reduced to synonymy with Sargassum.

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F. Liu et al.

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Table 1. Mitochondrial genome organization of S. fusiforme (Sf. KJ946428) with comparison to S. muticum (Sm. KJ938301) and S. horneri (Sh. KJ938300). % identity (nt/aa)

Gene

Type

Location

Size (bp) Sf/Sm/Sh

Sf/Sm

Sf/Sh

Sm/Sh

rnl (23S) trnK (uuu) trnV (uac) atp9 trnM1 (cau) trnL1 (uaa) trnH (gug) trnC (gca) trnN (guu) trnF (gaa) rps8 rpl6 rps2 rps4 nad1 tatC trnW (cca) ORF41 trnM2 (cau) trnQ (uug) trnL2 (uag) rps12 rps7 nad4L trnL3 (caa) rpl14 rpl5 trnG (gcc) ORF129 rpl16 rps3 rps19 rpl2 rps13 rps11 trnY (gua) cox3 atp6 trnR (ucu) nad2 cox1 trnI1 (gau) trnE (uuc) nad9 cob cox2 nad4 trnI2 (uau) nad5 nad6 nad11 nad3 rps14 atp8 trnS1 (gcu) trnD (guc) trnA (ugc) rps10 trnS2 (uga) rpl31 rns (16S) rrn5 (5S) trnM3 (cau) nad7 trnP (ugg)

rRNA tRNA tRNA CDS tRNA tRNA tRNA tRNA tRNA tRNA CDS CDS CDS CDS CDS CDS tRNA CDS tRNA tRNA tRNA CDS CDS CDS tRNA CDS CDS tRNA CDS CDS CDS CDS CDS CDS CDS tRNA CDS CDS tRNA CDS CDS tRNA tRNA CDS CDS CDS CDS tRNA CDS CDS CDS CDS CDS CDS tRNA tRNA tRNA CDS tRNA CDS rRNA rRNA tRNA CDS tRNA

1–2663 2786–2859 2871–2942 3010–3237 3297–3369 3378–3461 3473–3546 3552–3624 3625–3697 3724–3796 3803–4171 4168–4659 4659–5258 5248–6066 6114–7094 7005–7805 7825–7897 7946–8071 8111–8183 8210–8281 8284–8365 8369–8755 8749–9309 9319–9621 9629–9710 9717–10,097 10,102–10,635 10,655–10,727 10,761–11,150 11,154–11,567 11,536–12,396 12,398–12,640 12,627–13,373 13,404–13,763 13,753–14,262 14,274–14,355 14,369–15,187 15,274–16,023 16,061–16,133 16,138–17,622 17,627–19,213 19,285–19,356 19,388–19,459 19,548–20,117 20,132–21,391 21,418–24,561 24,552–26,000 26,046–26,117 26,121–28,106 28,091–28,882 28,875–29,495 29,503–29,865 29,862–30,152 30,251–30,412 30,441–30,528 30,547–30,619 30,638–30,710 30,790–31,110 31,125–31,208 31,219–31,431 31,596–33,128 33,135–33,270 33,268–33,342 33,363–34,559 34,592–34,663

2663/2665/2667 74/74/74 72/72/72 228/228/228 73/73/73 84/84/84 74/74/74 73/73/73 73/73/73 73/73/73 369/369/369 492/492/492 600/600/600 819/816/816 981/981/981 801/774/777 73/73/73 126/120/126 73/73/73 72/72/72 82/82/81 387/387/387 561/543/561 303/303/303 82/82/82 381/381/381 534/534/534 73/73/73 390/396/390 414/414/414 861/846/846 243/243/237 747/747/747 360/360/360 510/510/510 82/82/82 819/819/819 750/750/750 73/73/73 1485/1485/1485 1587/1587/1587 72/72/72 72/72/72 570/570/570 1260/1257/1257 3144/3141/3147 1449/1449/1449 72/72/72 1986/1986/1986 792/789/780 621/624/624 363/363/363 291/291/291 162/162/162 88/88/88 73/73/73 73/73/73 321/342/321 84/84/84 213/213/213 1533/1530/1536 136/126/136 75/75/75 1197/1197/1197 72/72/72

94.1/– 97.2/– 100.0/– 95.6/98.6 93.1/– 97.6/– 100.0/– 89.0/– 91.7/– 94.5/– 89.7/92.6 85.9/82.8 86.0//86.9 89.3/92.6 90.1/98.1 82.7/80.0 100.0/– 81.1/78.0 95.8/– 100.0/– 90.2/– 90.6/96.0 85.2/84.9 92.7/98.0 100.0/– 90.8/92.0 86.3/83.0 95.8/– 81.8/76.3 87.4/84.6 86.8/89.1 88.8/88.7 89.1/90.7 91.6/92.4 85.8/83.4 98.7/– 90.8/96.3 91.6/95.9 100.0/– 90.8/94.1 93.0/98.1 95.8/– 94.4/– 90.5/92.0 89.8/94.5 84.8/82.5 89.7/95.2 94.4/– 90.8/96.5 88.2/86.3 88.1/96.1 92.2/98.3 83.5/86.4 93.2/98.1 97.7/– 94.5/– 97.2/– 81.2/79.6 96.4/– 81.2/77.1 95.2/– 85.2/– 94.6/– 88.9/95.9 100.0/–

94.2/– 94.5/– 98.6/– 96.0/100.0 91.7/– 96.4/– 97.2/– 86.3/– 94.5/– 94.5/– 91.0/93.4 84.9/82.8 87.0/86.9 87.5/91.1 91.4/97.5 79.1/74.0 95.8/– 88.0/82.9 95.8/– 95.8/– 85.3/– 91.4/95.3 86.0/82.7 94.3/98.0 97.5/– 88.1/90.4 85.3/82.4 94.5/– 83.8/75.9 85.5/84.6 83.8/84.2 83.9/86.2 86.4/85.4 88.3/84.0 80.1/76.3 100.0/– 90.4/95.9 90.9/95.5 100.0/– 88.4/92.3 90.8/97.7 97.2/– 93.0/– 89.4/94.1 87.8/94.2 82.7/78.1 88.4/95.2 95.8/– 89.4/96.0 83.1/80.9 89.1/94.2 90.3/97.5 87.6/89.5 92.5/92.4 96.5/– 91.7/– 87.6/– 85.3/83.0 96.4/– 81.2/74.2 94.8/– 86.7/– 96.0/– 88.9/96.7 100.0/–

94.7/– 97.2/– 98.6/– 96.0/98.6 90.4/– 96.4/– 97.2/– 91.7/– 94.5/– 95.8/– 90.5/92.6 86.1/85.8 86.5/85.9 88.4/93.3 89.7/97.8 82.1/75.9 95.8/– 85.8/87.8 94.5/– 95.8/– 92.6/– 89.6/94.5 83.0/83.3 92.7/100.0 97.5/– 88.4/91.2 86.7/82.4 95.8/– 79.5/68.7 86.4/86.8 86.2/86.1 86.4/87.5 85.5/87.5 85.0/83.1 81.7/73.9 98.7/– 91.8/95.9 91.0/95.9 100.0/– 91.1/95.7 90.8/97.7 98.6/– 90.2/– 88.4/94.7 88.8/94.7 82.8/80.1 88.0/94.8 98.6/– 88.9/95.7 84.5/84.3 88.9/94.6 90.9/97.5 87.2/90.6 93.2/94.3 96.5/– 89.0/– 90.4/– 82.1/81.4 100.0/– 82.6/77.1 95.3/– 83.8/– 93.3/– 87.8/95.7 100.0/–

It shows gene name, type, and location of S. fusiforme, and comparison of gene size in three Sargassum species, and their gene identity (%) of nucleotide (nt) and/or amino acid (aa) sequences. Gene names in bold indicate genes transcribed on the light strand, whereas others on the heavy strand.

Mitogenome of Sargassum fusiforme

DOI: 10.3109/19401736.2014.936417

Declaration of interest This work was supported by the 863 Hi-Tech Research and Development Program of China (No. 2012AA10A413), the National Natural Science Foundation of China (No. 41206146, 41176135), the Scientific Research Foundation for Outstanding Young Scientists of Shandong Province (No. BS2013HZ004), the Open Reseach Fund of Key Laboratory of East China Sea and Oceanic Fishery Resources Exploitation and Utilization, Ministry of Agriculture (No. K201311), and the Open Research Fund of Key Laboratory of Integrated Marine Monitoring and Applied Technologies for Harmful Algal Blooms, State Oceanic Administration (No. MATHAB201408). The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

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Supplemetary material available online Supplementary figure

Notice of Correction: In the version of this article published online on 3 July 2014, several calculation errors were identified. The data has been corrected in this version. The authors and editors apologise for any inconvenience caused.

Complete mitochondrial genome of the brown alga Sargassum fusiforme (Sargassaceae, Phaeophyceae): genome architecture and taxonomic consideration.

Sargassum fusiforme (Harvey) Setchell (=Hizikia fusiformis (Harvey) Okamura) is one of the most important economic seaweeds for mariculture in China. ...
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