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Article

The Complete Mitochondrial Genome of the Chemosymbiotic Lucinid Bivalve Pillucina pisidium (Dunker, 1860) Occurring in Seagrass Zostera marina Bed in a Lagoon in Jeju Island, Korea

by
Jong-Seop Shin
1,
Chi-une Song
2,
Hyeongwoo Choi
2,
Sung Hyun Yang
3,
Kae Kyoung Kwon
3,
Seong-il Eyun
2,* and
Kwang-Sik Choi
1,*
1
Department of Marine Life Science (BK 21 FOUR), Jeju National University, Jeju 63243, Republic of Korea
2
Department of Life Science, Chung-Ang University, Seoul 06974, Republic of Korea
3
Marine Biotechnology & Bioresource Research Department, Korea Institute of Ocean Scienceand Technology, Busan 49111, Republic of Korea
*
Authors to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2024, 12(5), 847; https://doi.org/10.3390/jmse12050847
Submission received: 8 April 2024 / Revised: 11 May 2024 / Accepted: 16 May 2024 / Published: 20 May 2024
(This article belongs to the Special Issue Biodiversity and Population Ecology of Marine Invertebrates)
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Abstract

:
Commonly found in tropic and subtropic seagrass beds, lucinid clams host sulfur-oxidizing bacteria within their gills. These symbionts are crucial in converting phytotoxic sulfide in the sediment into less harmful sulfate, thus enhancing the environment for seagrasses and associated biota. We recently uncovered small clams within a Zostera marina seagrass bed situated in a lagoon on Jeju Island, off the south coast of Korea. These bivalves, with shell lengths of up to 7 mm, exhibited distinct features, including thick and hypertrophied gills, inflated and ovoid shells with a shell height/shell length ratio of 0.99, and the absence of a sulcus on the external shell surface. These characteristics align closely with those of Pillucina pisidium, a lucinid clam species originally reported in Japan. Analysis of the cytochrome b gene partial sequences of the clams from Jeju Island revealed a 100% match with P. pisidium reported in Japan, confirming their identity. Moreover, we successfully assembled the complete mitochondrial genome of P. pisidium for the first time, revealing a circular genome spanning 21,059 bp. Additionally, we constructed a phylogenetic tree using 13 protein-coding genes (PCGs) extracted from the mitochondrial genome of P. pisidium. Notably, P. pisidium formed a distinct clade within the subclass Autobranchia alongside other lucinid clams in the phylogenetic tree. However, within the family Lucinidae, synteny analysis of the 13 PCGs revealed diverse gene arrangement patterns, indicating considerable divergence. This divergence underscores the need for an extensive examination of Lucinidae mitochondrial genomes to elucidate the phylogenetic ties more precisely within the family, highlighting P. pisidium’s distinct evolutionary path within the family Lucinidae.

1. Introduction

Chemosymbiosis constitutes a mutualistic relationship between marine invertebrates and chemolithoautotrophic bacteria, wherein the bacteria oxidize sulfide derived from the environment to produce organic carbons, subsequently transferring nutrients to their host organisms [1]. This phenomenon gained recognition with the initial discovery of mutualistic chemosymbiotic bacteria in the giant tube worm Riftia pachyptila, thriving in deep-sea hydrothermal vents approximately 2500 m deep near the Galapagos Islands. Subsequent research has revealed similar symbiotic associations between marine invertebrates and chemolithoautotrophic bacteria across diverse marine habitats [1,2,3]. Notably, this chemosynthetic symbiosis is particularly prevalent among marine bivalves, with numerous species in families such as Mytilidae, Lucinidae, Thyasiridae, and Solemyidae harboring symbiotic bacteria within their gill tissues [3,4,5,6]. These chemosynthetic marine bivalves inhabit a wide array of marine environments, ranging from deep-sea hydrothermal vents and cold seeps to hypoxic intertidal zones and seagrass beds. In these habitats, chemical substrates like sulfide and methane are continuously supplied to the symbionts, serving as fuels for the production of organic matter [7,8,9,10,11,12].
The Lucinidae family represents one of the most diverse groups of chemosynthetic bivalves found across a range of marine habitats, spanning from deep-sea hydrothermal vents to seagrass beds and mangrove forests within tropical and subtropical estuaries and lagoons [6,13,14]. Predominantly, lucinid clams are obligate chemosymbionts, relying on symbiotic bacterial production for sustenance. These clams harbor sulfur-oxidizing gammaproteobacteria within specialized bacteriocytes located in their gill filaments, where the symbiotic bacteria oxidize sulfide and synthesize organic matter that is then transferred back to the host [15,16,17,18]. In seagrass beds, lucinid clams often play critical roles in enhancing the subsurface sediment environment by converting toxic sulfide accumulated in the sediments into less harmful sulfate [12]. Furthermore, according to König et al. (2016) [19] and Petersen et al. (2016) [20], the chemosymbionts within lucinid clams, such as Lucinoma lucinalis and Codakia orbicularis in seagrass meadows, also facilitate the fixation of inorganic nitrogen into organic nitrogen, providing a readily available nutrient source for marine plants and animals.
Common in seagrass meadows, the lucinid clam Pillucina pisidium has a broad geographical distribution range from the southern Pacific region, encompassing Madagascar and eastern Australia, to the northwestern Pacific, including Japan, Korea, and Vladivostok, Russia [21,22,23,24,25]. Through analysis of fatty acid profiles and the sulfur-stable isotope, Zhukova et al. (1992) [26] and Kharlamenko et al. (2001) [27] have affirmed that P. pisidium in seagrass beds in Vladivostok, Russia, harbor chemolithoautotrophic bacteria, potentially pivotal in neutralizing phytotoxins accumulated in the seagrass bed sediments. Furthermore, various studies have documented the presence of P. pisidium in intertidal areas along the south coast and Jeju Island in South Korea [28,29,30]. Nevertheless, the molecular identification and phylogenetic affiliation of P. pisidium in Korean waters remain unresolved. Moreover, recent studies on the phylogeny of the Lucinidae family have primarily used nuclear genes (12S and 16S rRNA) and mitochondrial cytochrome b (COB) to construct phylogenetic trees [23,31]. These studies have reported that the genus Pillucina does not form a monophyletic group, which contrasts with its morphological classification [23,31]. This indicates that a more comprehensive approach, utilizing multiple genes, is necessary for a clearer and more accurate interpretation of the phylogeny within the Lucinidae family.
Mitochondria trace their origins back to a common ancestor approximately two billion years ago and have become ubiquitous among eukaryotic organisms [32]. Due to the accessibility of mitochondrial genomic DNA, with its abundance of copies and conservation across diverse taxa, mitochondrial gene sequences (mtDNA) have found extensive application in fields like molecular evolution, phylogenetics, and population genetics [33,34]. Notably, cytochrome c oxidase subunit I (COX1), among the most conserved protein-coding genes (PCGs) within the mitochondrial genome, has been extensively employed for efficient species identification and phylogenetic analyses [34,35,36]. Recent research has demonstrated that analyzing the entire mitochondrial genome yields more informative data than focusing solely on the COX1 gene [33,35]. Consequently, this study marks the first to document the mitochondrial genome of the chemosymbiotic Lucinidae bivalve P. pisidium, integrating morphological and ecological insights. Moreover, we conducted a phylogenetic analysis employing 13 PCGs within the family Lucinidae.

2. Materials and Methods

Sampling Effort. In July 2022, small clams were harvested from sediment approximately 10 cm deep near the rhizomes and roots of Zostera marina, forming a meadow in the Ojo-ri lagoon (33.47° N, 126.92° E) along the eastern coast of Jeju Island (see Figure 1). A steel core with a 25 cm diameter was employed to extract sediment samples to collect the clams. Subsequently, the sediment containing clams underwent sieving through a 1 mm mesh screen. At the laboratory, the shell length (SL, maximum distance on the anterior-posterior axis) and shell height (SH, maximum distance on the umbo-ventral axis) of the lucinid clams were measured using vernier calipers. Subsequently, the entire soft tissue was separated from the shell, and the wet tissue weight was determined using an electronic balance.
DNA Isolation, Next-Generation Sequencing and Mitochondrial Genome Assembly. Genomic DNA extraction was conducted from the foot tissue, considered an organ free of symbiont, for mitochondrial genomic analysis. Approximately 20 mg of foot tissue was excised, and DNA extraction followed the manufacturer’s protocol using the DNeasy Blood and Tissue Kit (QIAGEN, San Diego, CA, USA). Subsequently, a 151 bp paired-end DNA library (with an insert size of 550 bp) was prepared using a TruSeq DNA Nano kit (Illumina, San Diego, CA, USA). The sequencing procedure was carried out on a NovaSeq 6000 platform (Illumina), facilitated by DNAlink Inc. (Seoul, Republic of Korea). The raw sequencing data of the closely related species, P. pacifica, was obtained from the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) database (accession number: SRR131632239, Osvatic et al., 2021) [36] to compare the DNA sequence obtained in this study.
Raw sequence data underwent quality filtering using Trim Galore! (ver. 0.6.10) with the specified parameters: --quality 20, --length 120, and --max_n 0, as documented at (https://github.com/FelixKrueger/TrimGalore, assessed on 8 January 2024) [37]. Subsequently, de novo assemblies of the mitochondrial genomes for both P. pisidium and P. pacifica were generated using the metaSpades mode (k-mer length: 21, 33, and 55) of MitoZ (ver. 3.6) [38,39,40,41,42]. The assembled circular forms of the two circular mitochondrial genomes were annotated utilizing MITOS2 (ver. 2.1.6) [43], with visualization accomplished using Circos (ver. 0.69-8) [44].
Phylogenetic Analysis. We conducted a phylogenetic analysis utilizing 13 protein-coding genes (PCGs) extracted from 26 species, all of which have complete mitochondrial genome sequences available in the NCBI database. This investigation aimed to elucidate the phylogenetic relationships within the subclass Autobranchia, encompassing chemosymbiotic lucinid clams (as outlined in Table 1). Four species from the genus Solemya (subclass Protobranchia) were included as outgroup representatives. Multiple sequence alignments (MSA) of the 13 PCGs were performed using MAFFT (ver. 7.520) with default parameters [45]. Subsequently, we employed PartitionFinder2 (ver. 2.1.1), utilizing Akaike’s Information Criterion (AICc), along with the ‘--raxml’ option, to identify the optimal partitioning schemes and models of molecular evolution [46,47]. The best fit evolutionary models for each gene are as follows: ATP6, COX1, COX2, COX3, CYTB, ND1, ND2, ND3, ND4, ND4L, ND5, ND6 (GTR + I + G), and ATP8 (GTR + G).
Phylogenetic analyses were conducted through the integration of maximum likelihood (ML) and Bayesian inference (BI) methods. The ML tree was reconstructed using RAxML-ng (ver. 1.2.0) with 1000 bootstrap replicates [48]. For the BI tree, MrBayes (ver. 3.2.7) was employed [49]. Two independent Markov chain Monte Carlo (MCMC) runs were executed, each comprising 1 × 106 generations with sampling every 1000 generations. Additionally, 25% of the initial data were discarded as burn-in data. The ML and BI tree were visualized using FigTree (ver. 1.4.4) (http://tree.bio.ed.ac.uk/software/figtree, accessed on 22 February 2024).

3. Results and Discussion

Morphological and Molecular Identification. Morphologically, the overall shell shape of Lucinidae clams found in Jeju Island closely resembles the type specimens reported by Dunker (1861) [50] in Japan, identified initially as Lucina pisidium. The SL of the small white clams collected from the Z. marina beds in Jeju Island measures 7.0 mm, and the mean SH to SL ratio was 0.99, suggesting a rounded and expanded form (see Figure 2A,B). Furthermore, a single cardinal tooth on the left and two cardinal teeth on the right valve align with the shell features typical of the genus Pillucina (Figure 2C). The distinctive triangular ligament presents on both the left and right valves, along with the absence of an anterior lateral tooth on the right valve, further differentiate this species, clearly distinguishing it from other species within the genus Pillucina (Figure 2C).
The clams exhibited a single pair of gills covering the mantle (Figure 2D). The gills were dark brown in color, thick, and occupied 24% of the total shell inner space and 42% of the mantle area, indicating a wide surface area (Figure 2D). Additionally, the weight of the gills accounted for approximately 17% of the total tissue weight. Thick, dark brown gills are a typical characteristic of Lucinidae clams and serve as an effective habitat for symbiotic bacteria. In Lucinidae gills, the presence of a lateral zone densely populated with bacteriocyte-containing symbionts contributes to their thick and dark appearance [51,52]. The high gill-to-somatic tissue weight ratio in Lucinidae bivalves indicates their reliance on organic matter synthesized by gill symbionts as a major energy source. Several studies have reported that the chemosynthetic P. pisidium in seagrass beds exhibits a high gill weight ratio, a unique characteristic of lucinid clams [22,26,27]. The gill-to-total tissue weight ratio of the Lucinidae clam Lucinoma aequizonata, collected from 550 m depth at the sill of the Santa Barbara Basin USA, reaches up to 35% [52] and 32.5% in Loripes lacteus, inhabiting a seagrass bed in Corsica, France [53].
The similarity between the Lucinidae clam from Jeju Island and comparable nucleotide sequences in the National Center for Biotechnology Information (NCBI) was compared. The 1143 bp COB gene, extracted from the analyzed mitochondrial genome, showed 100% similarity with the 355 bp partial sequence (KF741678.1) of P. pisidium in Japan reported by Taylor et al. (2014) [23]. Based on the shell morphology and the COB gene sequences, we concluded that the lucinid clam occurring in the Z. marina seagrass bed on Jeju Island is P. pisidium.
Mitochondrial Genome Characterization. We generated a total of 213,214,754 paired-end raw sequence reads from P. pisidium. A quality filtering process that retained bases with a Q-score above 20 and forward-reverse reads of at least 120 in length yielded 210,719,044 reads (98.8%). Subsequently, the mitochondrial genome was constructed using filtered reads.
We successfully generated the complete mitochondrial genome of the Chemosymbiotic Lucinid Clam, P. pisidium from the lagoon in Jeju Island for the first time. This circular genome spanned 21,059 bp and contained a complete set of 37 genes, including 13 PCGs (i.e., COX1, COX2, COX3, COB, ND1, ND2, ND3, ND4, ND4L, ND5, ND6, ATP6, and ATP8), two rRNAs (12S rRNA, and 16S rRNA), and 22 tRNAs (Table 2 and Figure 3). The nucleotide composition of the mitochondrial genome was as follows: A: 23.78%; T: 39.68%; G: 24.73%; and C: 11.81%, with an A + T content of 63.46% and G + C content of 36.54%. The average length of the intergenic regions between coding sequences was 175 bp. The P. pisidium genome is longer than the average mitochondrial genome length of 17,693 bp in other three Lucinidae species, due to its extended intergenic regions (Table 1). The mitochondrial genome of P. pisidium has been registered in the NCBI as a reference sequence (accession number: NC_071184.1).
In this study, we also assembled the mitochondrial genome of P. pacifica distributed in the northern Atlantic coast of Australia after downloading the WGS Illumina sequence from the NCBI Sequence Read Archive (SRA) database (SRR131632239) reported by Osvatic et al. (2021) to compare the mitochondrial genomes of closely related species. The raw data downloaded for P. pacifica consisted of a total of 5,341,670 paired-end reads. After quality filtering, we obtained 2,297,300 clean reads (43%). The P. pacifica complete mitochondrial genome was circular with a total length of 16,819 bp. The mitochondrial genome contained a complete set of 37 genes, including 13 PCGs (COX1, COX3, ND4L, ND2, COX2, ND6, COB, ATP6, ND4, ND3, ND1, ATP8, and ND5), two rRNAs (12S rRNA and 16S rRNA), and 22 tRNAs (Table 3). The nucleotide composition of the mitochondrial genome was as follows: A: 25.85%, T: 42.25%, G: 22.38%, and C: 9.52%, with A + T and G + C contents of 68.10% and 31.90%, respectively. The average length of the intergenic regions between coding sequences was 53.8 bp (Table 3). The mitochondrial genome of P. pacifica was registered in the NCBI’s GenBank database (accession number: BK067723).
Phylogeny and Synteny. A phylogenetic tree was constructed using the nucleotide sequences of the 13 PCGs to investigate the phylogenetic relationships of P. pisidium. An additional phylogenetic tree was reconstructed using 25 mitochondrial genomes from bivalve species, including our assembled mitochondrial genome of P. pacifica, along with existing raw data sequences (Table 1). Upon examination, the subclass Autobranchia and its outgroup, the subclass Protobranchia, were delineated (Figure 4). Within Autobranchia, the infraclasses Pteriomorphia and Heterochonchia formed sister groups. However, despite being a member of Heterochonchia, Sinohyriopsis schlegelii was grouped as an outgroup to the rest of the Autobranchia. Additionally, each family formed appropriate clusters with high reliability (bootstrap value > 90; Bayesian posterior probability > 0.9) (Figure 4). These results were consistent with the topology observed in phylogenetic trees constructed using various marker genes from different clam species [54,55].
P. pisidium was grouped with three other species in the Lucinidae family. However, it did not form a sister group with P. pacifica despite belonging to the same genus. Instead, it formed a sister group with L. lacteus and Lucinella divaricate with intermediate supporting value (bootstrap value = 63; Bayesian posterior probability = 0.97), with P. pacifica as the outgroup (Figure 4). The similarity between P. pisidium and P. pacifica was analyzed using the Basic Local Alignment Search Tool for nucleotides (BLASTn) (ver. 2.13.0+) for the 13 PCGs. Despite belonging to the same genus, the two species exhibited low average identity (74.28%), suggesting significant divergence. This divergence likely contributes to the inability of the genus Pillucina to form a monophyletic cluster. Therefore, it is imperative to conduct further studies that incorporate more species to meticulously examine the phylogenetic relationships within the family Lucinidae, ensuring a thorough understanding of their evolutionary history.
Gene arrangement of 13 PCGs among the 26 clam species displayed a wide variety of patterns (right panel of Figure 4). Only certain species with relatively close phylogenetic relationships shared gene orders at the family level (Mytilidae, Pectinidae, Lucinidae, and Vesicomyidae) and consistent gene orders were observed at the genus level (Solemya and Calyptogena). However, P. pisidium and P. pacifica did not exhibit matching synteny among the 13 PCGs, despite belonging to the same genus. However, P. pisidium, which forms a sister group with two other species (L. lacteus and L. divaricata), had a distinct gene order within the family Lucinidae. Conversely, P. pacifica, an outgroup within the family Lucinidae, shared a gene arrangement with L. lacteus and L. divaricata.

4. Conclusions

We analyzed molecular biology data of the chemosymbiotic clam P. pisidium, which is distributed in Z. marina beds in a lagoon on the eastern coast of Jeju Island. The shell morphology of P. pisidium matched the type material and the thick and hypertrophied gills reflected the characteristics of chemosynthetic clams. Including P. pisidium, phylogenetic analyses utilizing all 13 PCGs from the mitochondrial genomes of Autobranchia reported to date revealed phylogenetic relationships similar to those found in previous studies. Additionally, synteny analysis of the 13 PCGs revealed some similarities within the same genus/family; however, diverse gene arrangement patterns were observed. Specifically, P. pisidium belonged to the Lucinidae family but did not form a sister group with P. pacifica, even though they belong to the same genus. Moreover, P. pisidium exhibited distinctive features, i.e., the length of the entire mitochondrial genome and the arrangement of the PCGs, within the Lucinidae family. Therefore, a comprehensive investigation of the mitochondrial genomes of Lucinidae species is necessary to clarify phylogenetic relationships within this group.

Author Contributions

Conceptualization, S.-i.E. and K.-S.C.; formal analysis, data curation, and methodology, J.-S.S., C.-u.S., S.H.Y. and H.C.; writing—original draft preparation, J.-S.S. and C.-u.S.; writing—review and editing, J.-S.S., S.-i.E. and K.-S.C.; project administration, K.K.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Korea Institute of Marine Science & Technology Promotion (RS-2022-KS221676) and the Marine Biotics Project (20210469) funded by the Ministry of Oceans and Fisheries, Korea.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The raw sequencing data of Pillucinia pisidinum, is available from the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) database (accession number: SRR28961031). The mitochondrial sequence of P. pisidinum is available from the NCBI RefSeq of NCBI under accession no. NC_071184. The mitochondrial sequence of Pillucinia pacifica is available from the NCBI GenBank accession No. BK067723.

Conflicts of Interest

The authors declare that they have no competing interests.

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Figure 1. Map showing the study area Ojo-ri lagoon on the east coast of Jeju Island, Korea. The dot indicates the seagrass Zostera marina bed where the lucinid clams were collected.
Figure 1. Map showing the study area Ojo-ri lagoon on the east coast of Jeju Island, Korea. The dot indicates the seagrass Zostera marina bed where the lucinid clams were collected.
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Figure 2. Pillucina pisidium. (A), External view of the shell valves. (B), Internal view of the shell valves. (C), Shell hinge, and teeth. (D), Gross anatomy of the highly developed gill after removal of the right valve and most of its corresponding mantle lobe. SL = 7.55 mm. Abbreviations: LV: left valve; RV: right valve; L: ligament; C: cardinal tooth; PLT: posterior lateral tooth; G: gill; AAM: anterior adductor muscle; PAM: posterior adductor muscle; MM: mantle margin.
Figure 2. Pillucina pisidium. (A), External view of the shell valves. (B), Internal view of the shell valves. (C), Shell hinge, and teeth. (D), Gross anatomy of the highly developed gill after removal of the right valve and most of its corresponding mantle lobe. SL = 7.55 mm. Abbreviations: LV: left valve; RV: right valve; L: ligament; C: cardinal tooth; PLT: posterior lateral tooth; G: gill; AAM: anterior adductor muscle; PAM: posterior adductor muscle; MM: mantle margin.
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Figure 3. The mitochondrial genome map of Pillucina pisidium inhabiting the Zostera marina bed of Jeju Island. The innermost blue bar plot represents GC content. The middle purple circle shows sequencing depth. The outermost circle depicts gene order: red for COX genes, blue for ATP synthase, purple for COB, and green for ND genes. The two rRNAs are in orange, and the 22 tRNAs are in gray.
Figure 3. The mitochondrial genome map of Pillucina pisidium inhabiting the Zostera marina bed of Jeju Island. The innermost blue bar plot represents GC content. The middle purple circle shows sequencing depth. The outermost circle depicts gene order: red for COX genes, blue for ATP synthase, purple for COB, and green for ND genes. The two rRNAs are in orange, and the 22 tRNAs are in gray.
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Figure 4. The maximum likelihood (ML) phylogenetic tree of the subclass Autobranchia. The tree was reconstructed based on 13 protein-coding genes (PCGs). Four species in the genus Solemya were used as the outgroup. Bootstrap supports a value of >60% for ML (upper), and posterior probabilities of > 80% for Bayesian inference (BI) (lower) are indicated around each node. The background colors represent different infraclasses. The scale bar represents the relative substitution rates per site. Horizontal lines next to species names indicate members of the same family. The synteny of 13 mitochondrial PCGs was placed to the right of the tree. The horizontal bars to the left of the synteny and the dots next to the species names indicate the same order of 13 PCGs arrangement.
Figure 4. The maximum likelihood (ML) phylogenetic tree of the subclass Autobranchia. The tree was reconstructed based on 13 protein-coding genes (PCGs). Four species in the genus Solemya were used as the outgroup. Bootstrap supports a value of >60% for ML (upper), and posterior probabilities of > 80% for Bayesian inference (BI) (lower) are indicated around each node. The background colors represent different infraclasses. The scale bar represents the relative substitution rates per site. Horizontal lines next to species names indicate members of the same family. The synteny of 13 mitochondrial PCGs was placed to the right of the tree. The horizontal bars to the left of the synteny and the dots next to the species names indicate the same order of 13 PCGs arrangement.
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Table 1. GenBank accession list of the mitochondrial genomes of the 26 clams used in the analysis.
Table 1. GenBank accession list of the mitochondrial genomes of the 26 clams used in the analysis.
SubclassInfraclassOrderFamilySpecies NameAccession Number
AutobranchiaHeteroconchiaAdapedontaPharidaeSinohyriopsis schlegeliiAP018551.1
Sinonovacula constrictaEU880278.1
SolenidaeSolen grandisHQ703012.1
LucinidaLucinidaeLoripes lacteusEF043341.1
Lucinella divaricataEF043342.1
Pillucina pacificaBK067723
Pillucina pisidiumNC_071184.1
ThyasiridaeConchocele bisectaLC126312.1
MyidaDreissenidaeDreissena polymorphaMT483676.1
MyidaeMya arenariaMW727516.1
VeneridaVeneridaeRuditapes decussatusKP089983.1
VesicomyidaeCalyptogena magnificaKR862368.1
Calyptogena pacificaMT947386.1
Calyptogena rectimargoMT947387.1
PteriomorphiaArcidaArcidaeTegillarca granosaKJ607173.1
MytilidaMytilidaeBathymodiolus brooksiMT916743.1
Gigantidas platifronsAP014561.1
Mytilus galloprovincialisDQ399833.1
OstreidaOstreidaeCrassostrea gigasAF177226.1
PectinidaPectinidaeArgopecten irradiansEU023915.1
Mizuhopecten yessoensisAB271769.1
Pecten maximusKP900975.1
Protobranchia-SolemyidaSolemyidaeSolemya elarraichensisKY244079.1
Solemya pervernicosaKY244080.1
Solemya velesianaNC_034906.1
Solemya velumJQ728447.1
Table 2. Annotation of the Pillucina pisidium mitochondrial genome.
Table 2. Annotation of the Pillucina pisidium mitochondrial genome.
GenePositionLength (bp)Initiation CodonStop CodonIntergenic
Nucleotide (bp)
Cytochrome c oxidase subunit I (COX1)1–15361536ATGTAA2112
tRNA-Phe (trnF)2973–303967 1436
tRNA-Lys (trnK)3109–317365 69
tRNA-His (trnH)3185–324460 14
Cytochrome c oxidase subunit III (COX3)3257–4054798ATGTAG12
tRNA-Met (trnM)4105–417369 50
NADH dehydrogenase subunit 4L (ND4L)4239–4517279ATGTAA65
Cytochrome c oxidase subunit II (COX2)5243–6118876ATATAA725
tRNA-Ser (trnS2)6145–620965 26
NADH dehydrogenase subunit 6 (NAD6)6210–6704495ATTTAG0
Cytochrome b (COB)6709–78511143ATGTAA4
ATP synthase F0 subunit 6 (ATP6)7870–8574705ATTTAA18
tRNA-Leu (trnL1)8594–866067 19
tRNA-Glu (trnE)8916–898065 255
12S ribosomal RNA (rrnS)8994–9808815 13
NADH dehydrogenase subunit 4 (NAD4)9854–11,1941341ATTTAA45
tRNA-Asn (trnN)11,230–11,30172 35
tRNA-Asp (trnD)11,343–11,41169 41
tRNA-Pro (trnP)11,426–11,49368 14
tRNA-Trp (trnW)11,509–11,58274 15
tRNA-Gly (trnG)11,589–11,65668 6
tRNA-Arg (trnR)11,667–11,73569 10
tRNA-Thr (trnT)11,738–11,80265 202
tRNA-Val (trnV)11,819–11,88567 16
tRNA-Leu (trnL2)11,903–11,97169 17
NADH dehydrogenase subunit 3 (NAD3)11,972–12,319348ATTTAG0
tRNA-Ile (trnI)12,369–12,43567 49
16S ribosomal RNA12,435–13,5961162 −1
tRNA-Tyr (trnY)13,597–13,67680 0
RNA-Ala (trnA)13,820–13,88364 143
tRNA-Gln (trnQ)13,887–13,95266 3
ATP synthase F0 subunit 8 (ATP8)13,975–14,088114ATTTAA22
NADH dehydrogenase subunit 5 (NAD5)14,161–15,8911731ATATAA72
NADH dehydrogenase subunit 1 (NAD1)16,389–17,342954ATGTAA497
tRNA-Cys (trnC)17,402–17,46463 59
tRNA-Ser (trnS1)17,830–17,89768 366
NADH dehydrogenase subunit 2 (NAD 2)17,949–18,947999ATATAA51
Table 3. Annotation of the Pillucina pacifica mitochondrial genome.
Table 3. Annotation of the Pillucina pacifica mitochondrial genome.
GenePositionLength (bp)Initiation CodonStop CodonIntergenic
Nucleotide (bp)
Cytochrome c oxidase subunit I (COX1)1–15571557TTGTAA4
tRNA-Thr (trnT)1610–167970 52
tRNA-Pro (trnP)1681–174767 1
tRNA-Phe (trnF)1770–183667 22
tRNA-Lys (trnK)1851–191464 14
tRNA-His (trnH)1921–198565 6
Cytochrome c oxidase subunit III (COX3)1996–2793798ATGTAA10
tRNA-Met (trnM)2814–288370 20
NADH dehydrogenase subunit 4L (ND4L)2947–3234288ATGTAA63
tRNA-Ser (trnS1)3248–331669 13
NADH dehydrogenase subunit 2 (NAD2)3369–43701002ATTTAG52
Cytochrome c oxidase subunit II (COX2)4377–5312936TTGTAG6
tRNA-Val (trnV)5331–539565 18
tRNA-Ser (trnS2)5410–547263 14
NADH dehydrogenase subunit 6 (NAD6)5480–5972493ATTTAA7
Cytochrome b (COB)5973–71061134ATGTAG0
ATP synthase F0 subunit 6 (ATP6)7136–7781646ATATAA29
tRNA-Glu (trnE)8780–884566 998
tRNA-Trp (trnW)8889–895466 43
NADH dehydrogenase subunit 4 (NAD4)8973–10,3311359ATTTAA18
tRNA-Tyr (trnY)10,521–10,58464 189
tRNA-Leu (trnL1)10,595–10,66167 10
12S ribosomal RNA (rrnS)10,682–11,511830 20
tRNA-Arg (trnR)11,578–11,64871 66
tRNA-Leu (trnL2)11,766–11,83368 117
NADH dehydrogenase subunit 3 (NAD3)11,833–12,180348ATATAG-1
tRNA-Ile (trnI)12,191–12,25868 10
16S ribosomal RNA (rrnL)12,289–13,4551167 30
NADH dehydrogenase subunit 1 (NAD1)13,483–14,442960ATATAA27
tRNA-Asn (trnN)14,449–14,51365 6
tRNA-Gly (trnG)14,517–14,58367 3
tRNA-Gln (trnQ)14,616–14,69479 32
ATP synthase F0 subunit 8 (ATP8)14,702–14,815114ATTTAG7
tRNA-Ala (trnA)14,862–14,92867 46
tRNA-Cys (trnC)14,961–15,02363 32
NADH dehydrogenase subunit 5 (NAD5)15,025–16,7401716TTGTAG1
tRNA-Asp (trnD)16,748–16,81467 7
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Shin, J.-S.; Song, C.-u.; Choi, H.; Yang, S.H.; Kwon, K.K.; Eyun, S.-i.; Choi, K.-S. The Complete Mitochondrial Genome of the Chemosymbiotic Lucinid Bivalve Pillucina pisidium (Dunker, 1860) Occurring in Seagrass Zostera marina Bed in a Lagoon in Jeju Island, Korea. J. Mar. Sci. Eng. 2024, 12, 847. https://doi.org/10.3390/jmse12050847

AMA Style

Shin J-S, Song C-u, Choi H, Yang SH, Kwon KK, Eyun S-i, Choi K-S. The Complete Mitochondrial Genome of the Chemosymbiotic Lucinid Bivalve Pillucina pisidium (Dunker, 1860) Occurring in Seagrass Zostera marina Bed in a Lagoon in Jeju Island, Korea. Journal of Marine Science and Engineering. 2024; 12(5):847. https://doi.org/10.3390/jmse12050847

Chicago/Turabian Style

Shin, Jong-Seop, Chi-une Song, Hyeongwoo Choi, Sung Hyun Yang, Kae Kyoung Kwon, Seong-il Eyun, and Kwang-Sik Choi. 2024. "The Complete Mitochondrial Genome of the Chemosymbiotic Lucinid Bivalve Pillucina pisidium (Dunker, 1860) Occurring in Seagrass Zostera marina Bed in a Lagoon in Jeju Island, Korea" Journal of Marine Science and Engineering 12, no. 5: 847. https://doi.org/10.3390/jmse12050847

APA Style

Shin, J. -S., Song, C. -u., Choi, H., Yang, S. H., Kwon, K. K., Eyun, S. -i., & Choi, K. -S. (2024). The Complete Mitochondrial Genome of the Chemosymbiotic Lucinid Bivalve Pillucina pisidium (Dunker, 1860) Occurring in Seagrass Zostera marina Bed in a Lagoon in Jeju Island, Korea. Journal of Marine Science and Engineering, 12(5), 847. https://doi.org/10.3390/jmse12050847

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