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Article

Characterization of the Mitochondrial Genome, Ecological Distribution, and Morphological Features of the Marine Gastropod Mollusc Lophocochlias parvissimus (Gastropoda, Tornidae)

by
Minju Kim
1,2,†,
Hyeongwoo Choi
3,†,
Hyeon Kim
1,2,
Jiwon Kang
3,
Hyeon Gyeong Jeong
4,
Seong-il Eyun
3,* and
Jung-Hoon Kang
1,2,*
1
Ecological Risk Research Department, Korea Institute of Ocean Science and Technology, Geoje 53201, Republic of Korea
2
Department of Ocean Science, University of Science and Technology, Daejeon 34113, Republic of Korea
3
Department of Life Science, Chung-Ang University, Seoul 06974, Republic of Korea
4
Department of Taxonomy and Systematics, National Marine Biodiversity Institute of Korea, Seocheon 33662, Republic of Korea
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
J. Mar. Sci. Eng. 2023, 11(12), 2307; https://doi.org/10.3390/jmse11122307
Submission received: 31 October 2023 / Revised: 1 December 2023 / Accepted: 2 December 2023 / Published: 6 December 2023
(This article belongs to the Special Issue Recent Advances in Marine Mollusca: Evolutionary Biology and Molecular Phylogeny)
Browse Figures
Versions Notes

Abstract

:
The larvae of the marine gastropod Lophocochlias parvissimus are meroplankton that spend part of their lives as plankton that disperse and drift in the water column before settling on the sea floor. Two individuals of L. parvissimus larvae were sampled by the Multiple Opening/Closing Net and Environmental Sensing System (MOCNESS) from the Central Indian Ridge of the southwestern Indian Ocean in 2018 and 2019. We generated the first mitochondrial sequences for L. parvissimus, which will provide valuable genetic insight into the evolution of these organisms. In this study, we have determined that the mitogenome of L. parvissimus was 13,575 bp in length, consisting of 13 protein-coding genes, 18 tRNAs, and two rRNAs. Our work provides a new insight into the dispersal of L. parvissimus and previously missing components to the general understanding of the evolution of Truncatelloidea (Subclass Caenogastropoda).

1. Introduction

Meroplankton are larvae of benthic animals that spend part of their lives as plankton, and this phase in their lifecycle plays a critical role in dispersal distance [1]. Planktonic larvae are at the stage of being able to free swim, during which some species may feed, not only promoting dispersal but also colonization and resilience in the deep sea [2,3]. Meroplankton larvae may spend different temporal scales, from hours to weeks or months, in the phase of drifting and dispersing by the currents in the water column before settling and metamorphosing on the sea floor [4]. Meroplankton differ from holoplankton, which remain planktonic throughout their lives [5,6]. The distinct morphological features of gastropods are that the meroplankton of gastropods differ from holoplanktonic gastropods by their diamond-patterned shells with relatively large coils [5,6].
Lophocochlias parvissimus (Hedley, 1899), described as Liotia parvissima (Hedley, 1899), Parviturbo parvissimus (Hedley, 1899), and Parviturboides parvissimus (Hedley, 1899), has also appeared in the literature of Pilsbry (1921) as Haplocochlias (Lophocochlias) minutissimus [7,8]. The shell of L. parvissimus is small (diameter of 0.84 mm), solid, and turbinate, with a cream color, four whorls, and an umbilicus that is small, oblique, narrow, and deep [9]. L. parvissimus is commonly found in subtidal areas including the sediments of tide pools [10,11]. Small molluscs that are smaller in diameter than 10 mm are often in abundance and have great diversity [12]. The larvae of L. parvissimus are planktotrophic, so they are free-living and feed in the water column [11]. L. parvissimus are distributed across the Indo-Pacific region, including Hawaii, the Cocos-Keeling Islands, the Kiribati Republic, Fanning Island, the Line Islands from Jordan, Mozambique, Madagascar, Reunion, New Caledonia, the Loyalty Islands, Vanuatu, Fiji, Papua New Guinea, the Philippines, French Polynesia, and Western Australia’s tropical Kimberley region [12,13,14,15,16].
Tornidae is a family of small marine snails with operculum in the clade Littorinimorpha, including 30 genera [8]. The genus Lophocochlias has two species: L. parvissimus Hedley (1899) and L. procerus Rubio and Rolán (2015) [7,8,15]. These small molluscs are an important food source for benthic predators, and they are important grazers and bioturbators of sediments [12]. Most of the previous studies on L. parvissimus have focused on the adult species that live in the sediment or larvae in the coastal waters, so the dispersal and distribution of L. parvissimus in the larval stage in the open ocean have not yet been studied.
Mitochondria are characterized by unique features, including maternal inheritance, notable conservation, multiple copies within cells, a low sequence recombination rate, and a rapid evolutionary rate [17]. Due to these features, mitochondrial sequences are extensively utilized in phylogenetic research [18]. Compared to the other mitochondrial genes, cytochrome c oxidase subunit I (COX1) exhibits a more robust phylogenetic signal [19]. As of October 2023, despite their extensive use in various studies, no mitochondrial genome sequences from the family Tornidae had been publicly available. As mitochondrial genomes play a crucial role in phylogeny and evolutionary history, we generated mitochondrial genome sequences and assembled the mitochondrial genome of L. parvissimus. We present the first phylogenetic analysis to elucidate the evolutionary relationships of L. parvissimus within the family Tornidae.

2. Materials and Methods

Sample collection. The study was carried out in the water column above hydrothermal vent sites during 2018 and 2019, as part of the expedition conducted by the Korea Institute of Ocean Science and Technology (KIOST) to the Central Indian Ridge on board the R/V ISABU (Figure 1 and Table 1). All the samples were obtained from hydrothermal vents of the Onnuri Vent Field (OVF), Solitaire Field (SF), and Station A in June 2018 and OVF and Station B in July 2019 [5,20]. Stations A and B served as control sites in the northern region, outside the immediate influence of the hydrothermal vents. Site selection was informed by the direction of meridional Ekman flows, in which the water is transported from the northern area to the southern area during the boreal summer monsoon (Figure 1) [21].
The physical properties of the sites were measured using sensors (Sea-bird Electronics, Bellevue, WA, USA) of conductivity, temperature, and depth. Sensors were attached to an environmental sensing and sample collection system that employs a network of mesh nets that can be opened or closed at the discretion of the operator in order to control the timing of collection and maintain sample quality (Multiple Opening/Closing Net and Environmental Sensing System, MOCNESS; Biological environmental sampling systems Inc., BESS, Falmouth, MA, USA). The seawater samples for the analysis of chlorophyll a (chl a) concentration were obtained using Niskin bottles (PVC) mounted on the Rosette sampler. The chl a concentration water samples were not collected at stations A and B due to limited sampling time. The analysis of chl a concentrations was carried out at 5 depths, including the layers of surface and subsurface chlorophyll maximum. Seawater samples were filtered (47 mm GF/F, Whatman, GE Healthcare, Marlborough, MA, USA) under low vacuum pressure (<125 mmHg). The GF/F filters were frozen (−80 °C) until the extraction of samples in acetone (90%) at 4 °C in the dark for two days. Chl a concentration was determined using a fluorometer that was calibrated using Turner Designs chl a standard solution (Turner Designs, San Jose, CA, USA), as described by Parsons et al. (1984) [22]. The chl a concentrations data were integrated for all depths from surface to 200 m.
The zooplankton samples, including L. parvissimus larvae, were collected with a MOCNESS equipped with 200 µm mesh nets. The sensors of pressure, conductivity, and temperature were mounted on MOCNESS (Sea-Bird Electronics, USA). The deep-tow winch was used to attach MOCNESS, and the winch wire speed during the pay-out and haul-in was 20–30 m min−1. The vessel speed was kept between 1.5 and 2.0 knots during towing, and the net angle was maintained at the optimum angle of 45° for optimal sampling. Oblique tows after the deployment of MOCNESS to 100 m above the bottom were carried out to collect samples, and the sampling strata were divided into 5–7 layers (Table 1). The flowmeter attached to the MOCNESS was used to calculate the volume of filtered water. The MOCNESS sampling was successful in 2018. However, the process of collecting samples was more challenging in 2019, probably due to bad weather conditions that led to tangled nets at the depth layers 400–700 m, 700–1000 m, 1000–1300 m, and 1300–1600 m in the OVF (Table 1).
Zooplankton samples collected in cod-end buckets were transferred to sampling bottles that were further divided into two groups, in which one was fixed with borax-neutralized formalin (final concentration of 5%) for microscopic examination and the other sample was fixed with ethanol (99.9%) and was stored at –20 °C for further molecular analysis. Identification of L. parvissimus larvae was carried out under a stereomicroscope at 10×–80× magnification by isolating specimens with the same morphological features (Discovery V8, SteREO, Zeiss, Oberkochen, Germany). Photographs of the L. parvissimus samples were taken using a camera coupled to the stereoscope at 80× magnification (AxioCam ICc 3, Zeiss, Oberkochen, Germany). The total number of individuals was converted to individuals 100 m−3 (ind 100 m−3). The larvae of L. parvissimus derived from the ethyl-alcohol samples were sorted by morphological characteristics that were previously stated by Hedley, 1899 [9]. The confirmation of the species identification was conducted using genomic DNA extraction methods.
Next-generation sequencing and mitochondrial genome assembly. Whole genomic DNA was extracted using a QIAGEN Blood & Cell Culture DNA Mini Kit (QIAGEN, Hilden, Germany), according to the manufacturer’s instructions. Then, a 150 bp paired-end reads library was constructed using the TruSeq DNA Nano 550 bp kit (Illumina, Inc., San Diego, CA, USA) and sequenced with the Novaseq6000 platform (Illumina).
Quality control was performed using Trim Galore! (ver. 0.6.10) (https://www.bioinformatics.babraham.ac.uk/projects/trim_galore, accessed on 30 October 2023) with the following parameters [23,24]; -quality 20 -length 120 -max_n 0.
Then, we carried out de novo assembly using MitoZ (ver. 3.4) [25] to generate the mitochondrial genome sequence of L. parvissimus. Next, annotation of protein-coding genes (PCGs) was performed using the MITOS1 (http://mitos.bioinf.uni-leipzig.de/index.py, accessed on 30 October 2023) and MITOS2 web servers () and visualized by Circos (ver. 0.69–8) [26].
Phylogenetic analysis. To delineate phylogenetic relationships, we utilized both the cytochrome c oxidase subunit I (COX1) gene and 13 protein-coding genes (PCGs). In the COX1 data, we used sequences from 16 species of Truncatelloidea obtained from the National Center for Biotechnology Information (NCBI) nucleotide database. Haliotis discus hannai was used as an outgroup species (Table 2). The multiple sequence alignments (MSA) were generated using MAFFT (ver. 7.475) [27]. To identify the best-fit evolutionary model, we used ModelFinder implemented in IQ-TREE (ver. 2.2.0.3) based on the Bayesian information criterion [28]. The COX1 dataset best fits the GTR + F + I + G4 evolutionary model.
Within the 13 PCGs dataset, we concatenated 13 genes from seven mitochondrial genome sequences. Specifically, five sequences were derived from Littorinimorpha, while two were sourced from Neogastropoda and used as outgroups. The MSA for the 13 PCGs was performed utilizing MAFFT. Subsequently, the optimal partitioning scheme and best evolutionary models for each gene were determined using PartitionFinder (ver. 2.1.1) based on the Bayesian information criterion [29].
Maximum likelihood (ML) phylogeny tree was constructed using raxml-ng (ver. 0.9.0) [30]. Bayesian Inference (BI) tree was reconstructed using Mrbayes (ver. 3.2.4) [31]. We conducted 1000 bootstrap replicates in the ML analysis to ensure robustness and reliability. We employed two independent Markov chain Monte Carlo (MCMC) runs for the BI method, each comprising 1 × 106 generations. Sampling was performed every 500 generations, and an initial 25% of the samples were discarded as burn-in to ensure the convergence of the chains. The ML tree topology with bootstrapping support values (BS) from ML and Bayesian posterior probabilities (BPP) from BI on each node was visualized by FigTree (ver. 1.4.4) (http://tree.bio.ed.ac.uk/software/figtree, accessed on 30 October 2023).

3. Results and Discussion

Using MOCNESS sampling, a total of two representative L. parvissimus larvae were identified: one was retrieved from a depth of 0–100 m at Station A in 2018 and one from the 0–200 m depth range at OVF in 2019 (Figure 2). Small molluscs that are usually less than 10 mm in diameter are known to be important as a food source for benthic predators and also important grazers of sediments [12]. In this study, the two specimens of L. parvissimus larvae had a mean diameter of 398.4 µm and a mean height of 356.3 µm (Figure 2). The distribution of L. parvissimus larvae, expressed in cubic meters, was 0.4 ind. 100 m−3 and 0.3 ind. 100 m−3 at Station A and OVF, respectively (Table 1). In the stations where L. parvissimus appeared, the average temperature and salinity were 25.3 °C and 34.8 for 0–100 m at Station A during 2018 and 22.3 °C and 35.0 for 0–200 m at OVF during 2019 (Table 1). The integrated chl a concentrations were 18.9 mg m−3 at OVF during 2019 (Table 1).
The morphology of the L. parvissimus specimens retrieved in this study had the same features as previously described by Hedley (1899). The shell was solid with a yellowish-cream color and four whorls, and the umbilicus was small and oblique. L. parvissimus are known to have minute but solid shells that are tall for the family; the protoconch is multispiral or paucispiral and brown or white; the keel is a strong acute spiral, and the color is translucent white [9,15]. The specimen’s morphology was similar to that represented in the microscopic photograph image of KimMoll18, WAM S94346, depicted in Figure 4B of Middelfart et al. (2020), who sampled the organism from the shallow marine environments of the tropical Kimberley region, Western Australia. According to Middelfart et al. (2020), L. parvissimus was the second most common species after Parashiela cf. invisibilis [12]. Also, the morphological characteristics of L. parvissimus resembled photographs of L. minutissimus in Figure 1A–H of Rubio and Rolán (2015). The diameter of L. minutissimus ranged from 0.84 to 1.08 mm (mean: 0.96 mm) in their study, which was approximately 2.4 times larger than the specimen of L. parvissimus (mean: 0.40 mm) described in this study. From the size of the L. parvissimus specimens, we can assume that they are larvae that may have dispersed from the nearby seabed in this study.
Lophocochlias parvissimus is subtidal and is commonly found in sediments to a depth of 30 m in tide pools around the bases of seaweeds [10,11]. The species of Lophocochlias are known to be intertidal, and their bathymetric range is between 0 and 60 m [15]. The specimens found in greater depths of deep water might have occurred due to the dragging effect of surrounding currents [15]. The geographical distribution is broad, and they can colonize on all types of substrates, including hard and soft bottoms such as rocky, sandy, and muddy bottoms with corals and coarse sand [15]. The planktotrophic larvae of Lophocochlias are free-living and, in the adult period, are not reported to be commensal with burrowing invertebrates. They are an epifaunal species that feed on detritus [11]. Interestingly, L. parvissimus was observed in the open ocean (Station A and OVF), approximately 1500 km away from the small islands of Seychelles, Mauritius, and Reunion and 2200 km away from the larger islands of Madagascar and Sri Lanka. Two assumptions can be made from the results of this study. First, it may be possible that L. parvissimus may live in the deep sea, represented by a bottom depth of 1429–2111 m at our study sites. Second, it is more likely that the larvae of L. parvissimus may be dispersed from coastal areas of nearby islands to the upper 100~200 m of the study sites by complex surface currents in the western Indian Ocean. This species is distributed across the majority of the Indo-Pacific region, including islands of the Pacific such as Hawaii, Kiribati, New Caledonia, the Loyalty Islands, Vanuatu, Fiji, Papua New Guinea, the Philippines, French Polynesia, and islands of the Indian Ocean, such as Madagascar, Reunion, and the western part of Australia [12,13,14,16,32,33,34,35], and from the open ocean along the Central Indian Ridge of the southwestern Indian Ocean in the present study.
This study generated a dataset of 353,133,548 raw reads through Illumina paired-end sequencing from L. parvissimus. A stringent quality filtering procedure, defined by a Phred quality score greater than 20 (see the Material and Methods section), was employed. As a result, we retained 342,701,216 filtered reads, which comprised 97.05% of the initial dataset. Subsequently, these filtered reads were utilized to assemble the mitochondrial genome of L. parvissimus.
Here, we have generated the first mitochondrial genome of the Tornidae species. The mitochondrial genome of L. parvissimus is 13,575 bp in length and contains 36 genes, including 13 PCGs (COX1, COX2, COX3, CYTB, ND1, ND2, ND3, ND4, ND4L, ND5, ND6, ATP6, and ATP8), 2 rRNAs (s-rRNA and l-rRNA), and 18 tRNAs (Figure 3). However, four tRNA genes were absent in the mitochondrial genome of L. parvissimus. This was because the genomic materials were extracted from small-sized larvae, potentially imposing limitations on obtaining sufficient mitogenomes for assembly. The overall base composition of the mitochondrial genome was 36.57% (A), 25.28% (T), 21.34% (C), and 16.8% (G). The proportion of A + T (61.85%) was ~1.62 times higher than that of G + C (38.14%).
To elucidate phylogenetic relationships, we attempted to utilize the mitochondrial protein-coding genes. When constructing phylogenetic trees, it is usually more informative to choose several genes from across species and families rather than a single gene. However, the lack of complete mitochondrial genome sequences in the family Tornidae hindered the use of the 13 protein-coding genes. As an alternative approach, we used COX1 to construct a phylogenetic hypothesis. Nevertheless, this study is significant in providing the first mitochondrial sequence of L. parvissimus in the Tornidae, elucidating the taxonomic relationship at the genus level. L. minutissimus (GenBank accession No. LC598190) is currently accepted as L. parvissimus in WoRMS, and tree topology indicates species identity (Figure 4). A similarity search using blastn showed 99.04% identity between L. minutissimus and L. parvissimus, suggesting that they are conspecific. Our data indicated monophyly of Tornidae with strong support (BS = 100%, BPP = 1) and implied a sister-group relationship between Tornidae and Caecidae (BS = 62%, BPP = 0.9). Also, the phylogenetic tree robustly demonstrates nodal supports within the family (BS ≥ 86%, BPP = 1), excluding Tateidae (BS = 53%, BPP = 0.9).
In Figure 5, we found that the gene order remains consistent among six species belonging to the Littorinimorpha and Neogastropoda groups, except for L. parvissimus. Notably, the mitochondrial genome of L. parvissimus presents a distinctive modification in the syntenic arrangement involving the translocation of the ND3 and COX3 genes. However, the lack of comparative data makes it challenging to ascertain whether other species of Lophocochlias also exhibit this characteristic of gene relocation. Therefore, further studies are needed to incorporate additional mitochondrial data from Tornidae species to reconstruct a robust phylogenetic tree. Also, the utilization of 13 PCGs continues to be essential for achieving this objective.

4. Conclusions

Lophocochlias parvissimus were found in the epipelagic zones at Station A and OVF in the Central Indian Ridge. We conducted a comprehensive investigation into the ecological and molecular characteristics of L. parvissimus larvae and presented the first mitochondrial genome in the family Tornidae. Based on COX1, we constructed ML and BI trees to unveil the evolutionary and phylogenetic relationships of L. parvissimus larvae. Through our study, we discovered Tornidae forms a monophyletic group encompassing three genera: Lophocochlias, Pseudoliotia, and Elachorbis. Notably, we made a remarkable discovery during our investigation. The larvae of L. parvissimus were unexpectedly found in the upper 100–200 m of the epipelagic zone in the Central Indian Ridge at Station A and OVF. This finding suggests that the larvae might have been dispersed from nearby coastal areas in the Indian Ocean to offshore waters. Our study provided significant insight into L. parvissimus and its relationship within the family Tornidae. However, obtaining the whole mitochondrial genomes of other Tornidae species is required in future research to ensure a more robust and reliable phylogenetic study.

Author Contributions

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

Funding

This research was a part of the project titled “Understanding the deep-sea biosphere on seafloor hydrothermal vents in the Indian Ridge (No. 20170411)” funded by the Ministry of Oceans and Fisheries, Korea. This research was also supported by the Management of Marine Bio-resources and Systematic Research (MABIK 2023M00200) funded by the National Marine Biodiversity Institute of Korea and the Chung-Ang University Research Scholarship Grants in 2023.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The mitochondrial sequence of Lophocochlias parvissimus is openly available from the GenBank of NCBI (https://www.ncbi.nlm.nih.gov, accessed on 30 October 2023) under accession No. OR343907.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. The survey stations at the Central Indian Ridge. South Equatorial Current (SEC) and the direction of meridional Ekman transport (Me) cited from Hood et al. (2017).
Figure 1. The survey stations at the Central Indian Ridge. South Equatorial Current (SEC) and the direction of meridional Ekman transport (Me) cited from Hood et al. (2017).
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Figure 2. Microscopic photographs of Lophocochlias parvissimus larvae collected at Station A (2018) and OVF (2019). The scale bar indicates 100 µm.
Figure 2. Microscopic photographs of Lophocochlias parvissimus larvae collected at Station A (2018) and OVF (2019). The scale bar indicates 100 µm.
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Figure 3. Map of the Lophocochlias parvissimus mitochondrial genome. The inner (purple) and outer circles represent sequencing depth and gene arrangement, respectively. In the outer circle, 13 PCGs are marked in green, 2 rRNA genes are colored in orange, and 18 tRNA genes are denoted in red.
Figure 3. Map of the Lophocochlias parvissimus mitochondrial genome. The inner (purple) and outer circles represent sequencing depth and gene arrangement, respectively. In the outer circle, 13 PCGs are marked in green, 2 rRNA genes are colored in orange, and 18 tRNA genes are denoted in red.
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Figure 4. Maximum likelihood (ML) tree of the five families in Truncatelloidea using mitochondrial cytochrome c oxidase subunit I (COX1) sequences. The numbers on each node represent the bootstrap support values (BS) from ML and Bayesian posterior probabilities (BPP) from Bayesian inference (BI). The scale bar represents the number of substitutions per site.
Figure 4. Maximum likelihood (ML) tree of the five families in Truncatelloidea using mitochondrial cytochrome c oxidase subunit I (COX1) sequences. The numbers on each node represent the bootstrap support values (BS) from ML and Bayesian posterior probabilities (BPP) from Bayesian inference (BI). The scale bar represents the number of substitutions per site.
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Figure 5. The maximum likelihood (ML) tree was reconstructed based on 13 protein-coding genes (PCGs). We used seven mitochondrial genomes from Littorinimorpha and Neogastropoda. Two species from Neogastropoda (Nassariidae Reticulata and Purpura bufo) were used as the outgroup. The numbers on each node represent the bootstrap support values (BS) from ML and Bayesian posterior probabilities (BPP) from Bayesian inference (BI). The scale bar under the ML tree represents the number of substitutions per site. The mitochondrial gene arrangement was overlaid onto the ML tree. Measurements of the complete mitochondrial DNA length and the lengths of individual PCGs were not conducted in this result.
Figure 5. The maximum likelihood (ML) tree was reconstructed based on 13 protein-coding genes (PCGs). We used seven mitochondrial genomes from Littorinimorpha and Neogastropoda. Two species from Neogastropoda (Nassariidae Reticulata and Purpura bufo) were used as the outgroup. The numbers on each node represent the bootstrap support values (BS) from ML and Bayesian posterior probabilities (BPP) from Bayesian inference (BI). The scale bar under the ML tree represents the number of substitutions per site. The mitochondrial gene arrangement was overlaid onto the ML tree. Measurements of the complete mitochondrial DNA length and the lengths of individual PCGs were not conducted in this result.
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Table 1. The sampling strata and the environmental factors, including temp. (°C): average temperature, sal.: average salinity, chl a: integrated chlorophyll-a (mg m−3) concentrations, and total abundance of Lophocochlias parvissimus (ind. 100 m−3) at the sampling stations during 2018 and 2019 in the Central Indian Ridge. N.S.: not sampled.
Table 1. The sampling strata and the environmental factors, including temp. (°C): average temperature, sal.: average salinity, chl a: integrated chlorophyll-a (mg m−3) concentrations, and total abundance of Lophocochlias parvissimus (ind. 100 m−3) at the sampling stations during 2018 and 2019 in the Central Indian Ridge. N.S.: not sampled.
StationDate, TimeLongitude (°E),
Latitude (°S)		Bottom
Depth (m)		Sampling
Strata (m)		Temp.
(°C)		Sal.Chl a
(mg m−3)		Lophocochlias parvissimus Larvae (ind. 100 m−3)
A2018-06-26
02:40~07:11		67°10.45,
9°28.18		1429(1) 0–10025.334.8N.S.0.4
(2) 100–20015.835.0N.S.0
(3) 200–40011.834.9N.S.0
(4) 400–6008.634.7N.S.0
(5) 600–8007.334.7N.S.0
(6) 800–10006.334.7N.S.0
(7) 1000–13005.134.7N.S.0
Onnuri
Vent
Field		2018-06-24
04:25~09:07		66°24.42,
11°28.86		2374(1) 0–20022.035.013.50
(2) 200–50010.734.8N.S.0
(3) 500–10006.934.7N.S.0
(4) 1000–13004.934.7N.S.0
(5) 1300–16003.834.7N.S.0
(6) 1600–19003.034.7N.S.0
Onnuri
Vent
Field		2019-07-02
15:18~22:51		66°20.20,
11°20.61		2111(1) 0–20022.335.018.90.3
(2) 200–40011.934.6N.S.0
(3) 400–7008.234.7N.S.Tangled nets
(4) 700–10006.234.7N.S.Tangled nets
(5) 1000–13004.834.7N.S.Tangled nets
(6) 1300–16003.834.5N.S.Tangled nets
(7) 1600–19003.134.7N.S.0
B2019-07-04
20:52~23:05		67°10.88,
9°21.38		2126(1) 0–10026.023.2N.S.0
(2) 100–20015.925.8N.S.Tangled nets
(3) 200–30012.526.5N.S.Tangled nets
(4) 300–40011.326.7N.S.0
(5) 400–5009.726.8N.S.Tangled nets
Table 2. GenBank accession numbers of the cytochrome oxidase subunit 1 (COX1) from 17 gastropods.
Table 2. GenBank accession numbers of the cytochrome oxidase subunit 1 (COX1) from 17 gastropods.
SuperfamilyFamilySpeciesAccession Number
TruncatelloideaTornidaeLophocochlias parvissimusOR343907
Lophocochlias minutissimusLC598190.1
Pseudoliotia micansKC439806.1
Elachorbis subtateiKC439807.1
CochliopidaeHeleobia australisMT295126.1
Helebops docimusAF129322.1
Juturnia kosteriKF876283.1
Littoridinops tenuipesEF490566.1
IravadiidaeIravadia australisJX970607.1
Iravadia resimaKC439779.1
CaecidaeCaecum japonicumLC598181.1
Caecum tracheaKC439805.1
TateidaeSulawesidrobia bicolorHM587338.1
Potamopyrgus antipodarumMG979468.1
Fluviopupa breviorKC875085.1
Tatea rufilabrisKC439802.1
HaliotoideaHaliotidaeHaliotis discus hannaiJF748784.1
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Kim, M.; Choi, H.; Kim, H.; Kang, J.; Jeong, H.G.; Eyun, S.-i.; Kang, J.-H. Characterization of the Mitochondrial Genome, Ecological Distribution, and Morphological Features of the Marine Gastropod Mollusc Lophocochlias parvissimus (Gastropoda, Tornidae). J. Mar. Sci. Eng. 2023, 11, 2307. https://doi.org/10.3390/jmse11122307

AMA Style

Kim M, Choi H, Kim H, Kang J, Jeong HG, Eyun S-i, Kang J-H. Characterization of the Mitochondrial Genome, Ecological Distribution, and Morphological Features of the Marine Gastropod Mollusc Lophocochlias parvissimus (Gastropoda, Tornidae). Journal of Marine Science and Engineering. 2023; 11(12):2307. https://doi.org/10.3390/jmse11122307

Chicago/Turabian Style

Kim, Minju, Hyeongwoo Choi, Hyeon Kim, Jiwon Kang, Hyeon Gyeong Jeong, Seong-il Eyun, and Jung-Hoon Kang. 2023. "Characterization of the Mitochondrial Genome, Ecological Distribution, and Morphological Features of the Marine Gastropod Mollusc Lophocochlias parvissimus (Gastropoda, Tornidae)" Journal of Marine Science and Engineering 11, no. 12: 2307. https://doi.org/10.3390/jmse11122307

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