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Article

Mitochondrial and Plastid Genomes of the Monoraphid Diatom Schizostauron trachyderma

by
Ewa Górecka
1,*,
Romain Gastineau
1,*,
Nikolai A. Davidovich
2,
Olga I. Davidovich
2,
Matt P. Ashworth
3,
Jamal S. M. Sabir
4,
Claude Lemieux
5,
Monique Turmel
5 and
Andrzej Witkowski
1
1
Institute of Marine and Environmental Sciences, University of Szczecin, Mickiewicza 16a, 70-383 Szczecin, Poland
2
Karadag Scientific Station—Natural Reserve of the Russian Academy of Sciences, p/o Kurortnoe, Feodosiya, 98188 Crimea, Russia
3
Department of Molecular Biosciences, NHB, University of Texas at Austin, Austin, TX 78712, USA
4
Genomics and Biotechnology Research Group, Faculty of Science, King Abdulaziz University, Jeddah 21589, Saudi Arabia
5
Département de Biochimie, Microbiologie et Bio-Informatique, Institut de Biologie Intégrative et des Systèmes, Université Laval, Québec, QC G1V 0A6, Canada
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2021, 22(20), 11139; https://doi.org/10.3390/ijms222011139
Submission received: 1 September 2021 / Revised: 5 October 2021 / Accepted: 11 October 2021 / Published: 15 October 2021
(This article belongs to the Special Issue Chloroplast 3.0)
Browse Figures
Versions Notes

Abstract

:
We provide for the first time the complete plastid and mitochondrial genomes of a monoraphid diatom: Schizostauron trachyderma. The mitogenome is 41,957 bp in size and displays two group II introns in the cox1 gene. The 187,029 bp plastid genome features the typical quadripartite architecture of diatom genomes. It contains a group II intron in the petB gene that overlaps the large single-copy and the inverted repeat region. There is also a group IB4 intron encoding a putative LAGLIDADG homing endonuclease in the rnl gene. The multigene phylogenies conducted provide more evidence of the proximity between S. trachyderma and fistula-bearing species of biraphid diatoms.

1. Introduction

The genus Schizostauron Grunow [1] represents one of the heterovalvar lineages of diatoms, where the two primary shells (valves) which make up the siliceous cell wall (frustule) have differing morphologies. In the case of Schizostauron, only one valve possesses raphe—longitudinal slits at the center of the valve which are involved in motility. Diatoms with this particular kind of heterovalvy are called “monoraphids”, and the two valves are labelled by their raphe (RV) or lack of raphe (SV). Taxa in Schizostauron can be distinguished from other monoraphid genera by the morphology of the transverse thickening of silica at the central area of the RV called a stauros. The genus is typical of temperate to tropical marine littoral zones. Species in this genus have often been misidentified as the monoraphid genera Achnanthes or Cocconeis and have a complicated taxonomic history, which includes the registration of invalid holotypes [1,2,3,4,5].
Since the mid-19th century, monoraphid diatoms have been classified in a separate evolutionary lineage featuring one raphe-loss event [6,7,8,9]. Treated as such, all described monoraphid genera were assigned to the order Achnanthales, including Achnanthes (Achnanthaceae), Cocconeis, Campyloneis, Anorthoneis (Cocconeidaceae), Achnanthidium, and Eucocconeis (Achnanthidiaceae). Round et al. [8] later split the genus Achnanthes sensu lato into several genera based on the re-evaluation of distinctive and shared morphological characters. The presence of a heterovalvate frustule is a shared feature of all members of Achnanthes sensu lato, but other morphological characters such as the girdle, orientation and shape of areola, and valve outline or central area structure are highly variable. The process of transferring taxa from Achnanthes and Cocconeis sensu lato into morphologically appropriate, newly established genera has continued over the last three decades and multiple new genera have been established [10,11,12,13,14,15,16], but despite these revisions, small groups of achnanthoid and cocconeid taxa remain without detailed generic accommodation.
Molecular phylogenetic studies of the raphid diatoms have supported the idea of multiple switches to the monoraphid state. These studies have shown Schizostauron to be monophyletic and closely related to other monoraphid genera such as Astartiella, Madinithidium, Kolbesia, and Karayevia. However, these “stauroneid” monoraphid genera (so named because of the presence of Stauroneis Ehrenberg sensu stricto in the molecular clade) are not monophyletic with respect to the other monoraphid genera of the Achnanthaceae, Achnanthidiaceae, and Cocconeidaceae, suggesting that their monoraphid states evolved independently [4,5,17].
Among other discriminating morphological characters, Schizostauron and monoraphid species included in the stauroneid have coaxial internal proximal raphe ends. This character is universal for the stauroneid genera Stauroneis, Craticula [8], and others that were recently studied using molecular data such as Fistulifera, Proschkinia, and Sternimirus [18,19,20,21]. In contrast, the genera in the Achnanthidiaceae and Cocconeidaceae feature proximal raphe ends bent internally into opposite directions [8,22]. The monoraphid species clearly need a revision of the higher-level taxonomy as they fail to form a natural group [22,23,24]. In addition, this could bring us closer to understanding the evolutionary origins of the different monoraphid genera, which would be the first step to elucidating the ecological or molecular selective pressures which lead to heterovalvy.
Here, we report the mitochondrial and plastid genome sequences of Schizostauron trachyderma (F.Meister) Górecka, Riaux-Gobin, and Witkowski, the first organellar genomes of a monoraphid diatom. These genomic data strengthen the phylogenetic position recently reported by Górecka et al. [5] and reveal that Schizostauron forms a clade within the Stauroneidaceae that is a sister to fistula-bearing Fistulifera and Proschkinia taxa. Several unusual features of the S. trachyderma organellar genomes will be discussed.

2. Results

2.1. Microscopy

Figure 1 illustrates the morphology of S. trachyderma, both in LM and SEM. The monoraphid morphology is apparent in comparing Figure 1d,e,i (RV) with Figure 1f–h (SV). The transverse stauros on the RV is particularly obvious in LM on Figure 1d,e.

2.2. Mitochondrial Genome

The 41,957 bp mitogenome of S. trachyderma (GenBank accession MZ520767) was retrieved with a coverage of 112X. It encodes the genes for 2 rRNAs, 22 tRNAs, and 35 proteins that include the two subunits of Nad11 and the conserved orf147 [25] (Figure 2). Two group II introns of 3348 bp and 3325 bp in length interrupt cox1 and both code for putative reverse transcriptases (orf692 and orf679, respectively). The nad11-a and nad11-b genes are adjacent to each other and are separated by only a 139-bp intergenic sequence. Note that the exact position of the start codon of nad7 and rpl6 remains ambiguous.

2.3. Comparative Analysis of Diatom Mitochondrial Genomes

The mitochondrial genome of S. trachyderma was aligned to those of five closely related species identified in the phylogenetic analysis described below. In total, five blocks of synteny were detected in the MAUVE alignment (Figure 3). The mitogenome of S. trachyderma revealed a unique arrangement of these syntenic blocks, with the adjacent syntenic blocks formed by cob and by cox3, nad3, cox2, nad7, nad9, and rps14 rearranged to the opposite DNA strand as compared to the other five genomes. Two sets of colinear mitochondrial genomes were identified: (1) those of Berkeleya fennica Juhlin-Dannfelt and Didymosphenia geminata (Lyngbye) M. Schmidt; and (2) those of Fistulifera solaris S. Mayama, M. Matsumoto, K. Nemoto, and T. Tanaka, as well as Fistulifera saprophila (Lange-Bertalot and Bonik) Lange-Bertalot and Proschkinia sp. These two sets of colinear mitogenomes differ only with respect to the position of a large syntenic block containing atp6, rps10, rps8, rpl6, rps2, rps4, atp8, rps12, rps7, rpl14, rpl5, nad1, tatC, orf147, rps11, rpl2, rps19, rps3, rpl16, atp9, nad4L, nad11-a, and nad11-b. The significantly larger mitogenome of Proschkinia sp. is mostly explained by the presence of introns in cox1.

2.4. Plastid Genome

The 187,029 bp plastid genome of S. trachyderma (GenBank accession MZ520768) exhibits the typical quadripartite architecture of diatom genomes (Figure 4). The large single-copy (LSC) region was retrieved with a coverage of 217X. It is 92,894 bp in size and encodes 67 conserved proteins, 15 tRNAs, and 22 open reading frames (ORFs) (Table 1). The closely linked orf104a and orf134a show similarities to xerC sequences coding for the putative integrases/recombinases. The putative protein of orf134a corresponds to the C-terminal domain of the integrases/recombinases and displays three of the conserved amino-acid residues present in this region (His-289, Arg-292, and Tyr-324), whereas the predicted protein of orf104a corresponds to the N-terminal domain of the integrases/recombinases but lacks the conserved Arg-173 typically present in this region. We speculate that these two ORFs are pseudogenes originating from a single large reading frame that was once coding for a functional protein. The predicted protein of orf110a shows some similarities with serine recombinases (serC), but its sequence is incomplete, lacking the C-terminal DNA binding site. The other putative serC (orf224a and orf227a) and xerC (orf299a and orf418a) proteins encoded by the plastid genome of S. trachyderma appear complete. In contrast, for example, to the Haslea silbo Gastineau, Hansen, and Mouget plastid genome that recently revealed all serC and xerC sequences in a single ca. 30 kb fragment located between ycf35 and psbA [26], these elements are located in five distinct regions of the S. trachyderma (between the IR and psaJ, ycf90 and psbZ, psbB and rbcS, atpA and rps14, tsf and atpB).
The small single-copy (SSC) region of S. trachyderma was retrieved with a coverage of 222X. It is 59,661 bp in size, and encodes 52 conserved proteins, 7 tRNAs, and 16 non-conserved ORFs, some of which encode putative xerC (orf294a and orf317a) and serC (orf234a) integrases/recombinases. The predicted protein of orf112a also shows some similarities with xerC integrases/recombinases but only retains the conserved Arg-173 and lacks the C-terminal region. Note that most of the ORFs encoding putative integrases/recombinases are located in a single block between ycf46 and rps10.
The 17,237 bp inverted repeat (IR) region of the S. trachyderma plastid genome was retrieved with a coverage of 428X. It encodes nine proteins (psbY, ycf89, ycf45, rpl20, rpl35, psaE, ftsH, petD, petB), three rRNAs, three tRNAs, and three ORFs. The petB gene overlaps the IR and LSC regions and contains a 2287-bp group II intron coding for a putative reverse transcriptase (RT, orf494) that shows a high sequence similarity to the RTs identified in the same gene from the diatoms Nanofrustulum shiloi (J.J. Lee, Reimer, and McEnery) Round, Hallsteinsen and Paasche [27] and Halamphora calidilacuna J.G. Stepanek and Kociolek [28] (Table 1). Moreover, the introns of S. trachyderma, N. shiloi, and H. calidilacuna share the same insertion position between codons 7 and 8 of petB. Located between ftsH and petB of S. trachyderma, orf119 shows some similarities to serC sequences, but its N-terminal region is incomplete and lacks most of the presynaptic site 1 dimer interface.
The plastid gene for the large subunit ribosomal RNA (rnl) of S. trachyderma contains an IB4 intron of 657 bp that encodes a putative LAGLIDADG homing endonuclease (orf139). This intron is inserted between residues 1931 and 1932 relative to the 23S rRNA of Escherichia coli str. K-12, an insertion site that has been frequently observed among green algae [29,30]. The predicted protein of orf139 also shows strong similarity with the homing endonucleases identified in green algal IB4 introns at site 1931 [29]. As shown in the LOGO consensus of Figure 5, the typical QWIVGFVDG and PFFE motifs of LAGLIDADG homing endonucleases are highly conserved in the predicted protein of orf139.

2.5. Comparative Analyses of the Gene Content of Diatom Plastid Genomes

The gene contents of plastid genomes from all available raphid diatoms were compared with that of S. trachyderma; a comparative table adapted from previous work [31] is displayed as Figure 6. The LSC contains a copy of the tsf gene, which codes for translation elongation factor T and often seems lost among raphid pennates, found only in Fistulifera spp., D. geminata, Gomphoneis minuta var. cassiae Kociolek and Stoermer, and Phaeodactylum tricornutum Bohlin. With the exception of P. tricornutum, all these species belong to the same clade in the plastid multigene phylogeny presented below, but this clade also contains Climaconeis spp., among which this gene was not found [32]. None of the Bacillariaceae (Nitzschia spp., Tryblionella apiculata W.Gregory) or Naviculaceae (Haslea spp., Seminavis robusta D.B. Danielidis and D.G.Mann, Navicula veneta Kützing) present it, nor do Halamphora spp. However, based on previous works [31], this gene is also absent from almost three-quarters of the plastid genomes sequenced, including most centric and araphid pennate species. Schizostauron trachyderma possesses the two genes thiS and thiG, shared by all the other species of the cluster, except Fistulifera spp. Schizostauron trachyderma, which is missing the bas1/ycf42 gene. This gene is also missing among most Bacillariaceae and Naviculaceae but has been found in Nitzschia supralitorea Lange-Bertalot. Among the species clustered by phylogeny, only D. geminata presents a pseudogene version of bas1/ycf42.

2.6. Multigene Phylogenies

We inferred mitochondrial and plastid phylogenomic trees from the concatenated gene sequences of S. trachyderma and all raphid pennate diatom organelle genome sequences available in GenBank, using an araphid pennate species as an outgroup. Schizostauron trachyderma proved to be a sister to Fistulifera spp. (and Proschkinia sp. in the case of the mitochondrial data) in all trees (Figure 7 and Figure 8), a result consistent with recently reported phylogenetic analyses [5,20,21]. Note that Fistulifera and Proschkinia taxa present a distinctive occluded pore on their valves, called a fistula. Interestingly, this feature is not found on Schizostauron valves.
The mitogenome-based tree (Figure 7) is the most taxon-rich of both trees, mostly because of the availability of several mitogenomes from two genera of the Bacillariaceae (Nitzschia and Pseudo-nitzschia). In addition to the Schizostauron, Fistulifera, and Proschkinia association mentioned above, the mitochondrial tree revealed that S. trachyderma was part of a larger clade including Surirella sp., Halamphora spp., Entomoneis sp., P. tricornutum, D. geminata, and B. fennica. The Naviculaceae formed a monophyletic group sister to a clade containing the rest of the raphid pennates.
Although the plastome-based phylogenetic tree (Figure 8) has a smaller taxon sampling, its topology is similar to the mitochondrial tree. The S. trachyderma also proved to be a sister of Fistulifera spp. and these taxa were recovered in a clade that also includes G. minuta var. cassiae, D. geminata, and Climaconeis spp.

3. Discussion

The multigene phylogenetic analyses presented here confirm the close evolutionary relationship between S. trachyderma and fistula-bearing taxa such as Fistulifera spp. and Proschkinia sp. This phylogenetic association could be improved and refined in future studies of additional organellar genomes of monoraphid genera such as Astartiella, Madinithidium, Karayevia, and Kolbesia. Based on recently published analyses, we expect these genera to be related to Schizostauron, as these stauroneid monoraphid taxa form a monophyletic clade sister to Fistulifera and Proschkinia, which is nested in a clade comprising genera belonging to Stauroneidaceae, such as Stauroneis, Craticula, Sternimirus, Dorofeyukea, Parlibellus, and Prestauroneis [5,17,18,20,21]. It is possible that the close relationship of stauroneid biraphid genera to stauroneid monoraphid genera is a result of insufficient taxon sampling or inadequate or insufficient choice of molecular markers. Genomic data from these taxa might reveal signature characters of specific monoraphid clades and could provide insights to the independent losses of the raphe on one valve.
The S. trachyderma plastid genome revealed features that were rarely or never observed among diatoms. The finding of a group II intron overlapping the IR and the LSC regions in the petB gene is certainly noteworthy, as is the observation of a LAGLIDADG homing endonuclease in the rnl gene. To our knowledge, genes encoding this type of homing endonuclease have so far been found only in the IA3 rnl intron of the S. robusta plastid genome (annotated as I-SroI, accession AZJ16657.1 [33] and in a cox1 intron of the N. supralitorea mitogenome, accession QWM93242.1 [34]. As in a few other diatom species [31], our analyses of conserved domains in the putative serC and xerC genes of S. trachyderma suggest that some of them are pseudogenes. As interesting as both the above-mentioned results are for the study of mobile DNA, we refrain from speculating on any explanation regarding their presence/absence among different taxa.
Our study, the first of its kind on a monoraphid diatom, should soon be followed by more organellar genome sequencing on other species belonging to genera such as the aforementioned Parlibellus, Stauroneis, Astartiella, and Madinithidium.

4. Materials and Methods

4.1. Isolation and Cultivation of the Biological Material

The strain SZCZE1420 of S. trachyderma was isolated from an environmental sample collected in February 2015 near Jeddah on the Red Sea coast of Saudi Arabia (21.7561° N 39.05° E). A monoclonal culture was established using glass micropipettes and inverted light microscopy (Nikon eclipse TS100) following Andersen and Kawachi [35]. The culture is kept in artificial f/2 culture medium [36] in a growth chamber (Biogenet, Poland) with 12 h day (20 °C):12 h night (18 °C) cycles under 100 μmol photons m−2 s−1 illumination.

4.2. Light and Scanning Electron Microscopy

Diatom pellets were centrifuged at 900× g for 5 min and treated with 37% hydrogen peroxide for 3 h at 170 °C to remove organic components of frustules. The residual material was washed 7–10 times with distilled water. For light microscopy (LM), cleaned frustules were pipetted onto coverslips, air-dried, and mounted on glass slides with synthetic diatom resin Naphrax® (Brunel Microscopes Ltd., Chippenham, UK). LM microphotographs of cleaned frustules and plastids were taken at the University of Szczecin by means of a Zeiss Axio Scope A1 (Carl Zeiss, Jena, Germany) with an oil immersion lens Zeiss Plan-Apochromat 100×/1.40 Oil M27 (Carl Zeiss, Jena, Germany) using a Canon EOS 500D camera (Canon, Tokyo, Japan) with the Canon EOS Utility software. For scanning electron microscopy (SEM), the cleaned material was pipetted onto a Whatman Nuclepore polycarbonate membrane filter with 5 µm pores (cat. no. 110613, Maidstone, UK) and mounted onto aluminium stubs. SEM observations were performed using a Hitachi SU8010 (Tokyo, Japan) at the University of Rzeszów (Poland), Faculty of Agriculture and Biology.

4.3. DNA Sequencing, Annotation, Whole Genome Alignments and Phylogeny

The SZCZE1420 clone of S. trachyderma was grown as described above, and cells in the exponential growth phase were harvested by centrifugation. DNA was extracted according to Doyle and Doyle [37]. Sequencing took place on the DNBseq platform at the Beijing Genomics Institute (Shenzhen). A total of 40 million 150-bp paired-end reads were assembled using SPAdes 3.14.0 [38] with a k-mer of 125. Contigs were verified and merged using Consed [39]. The genes were identified as previously described [34,40]. Maps of organellar genomes were prepared using the OGDRAW v1.3.1 online platform [41]. Whole mitogenome alignment was performed with progressive Mauve [42] after removing the second copy of the IR sequence in the plastid genomes. LOGO consensus sequences of LAGLIDADG homing endonucleases were obtained online with WebLogo3 [43]. For multigene phylogenies, mitochondrial and plastid protein-coding genes were extracted, separately concatenated, and aligned with orthologous diatom gene sequences obtained from GenBank. The mitochondrial and plastid multigene phylogeny were conducted on 37 and 26 taxa, respectively, including S. trachyderma and U. acus in both cases. The sampling was restricted to raphid pennate species, except for the araphid species Ulnaria acus (Kützing) Aboal that served as an outgroup. Phylogenetic analyses were conducted using RaxML version 8 [44], with the GTR + I + G model and 1000 bootstrap replications. Genes were concatenated and aligned using MAFFT 7 [45] before the alignments were trimmed by trimAl v1.2 [46]. The evolution model was chosen using jModelTest2 v2.1.10 [47] on the trimmed alignments. The number of concatenated genes was 35 for the mitochondrial-inferred phylogeny and 127 for the plastid-inferred phylogeny. The final sizes of the alignments as calculated by trimAl were 22140 bp for the mitochondrial genes alignment and 86587 bp for the plastid genes alignment. The evolution model was used as a single model across the entire alignment.

Author Contributions

Conceptualization, E.G. and R.G.; funding acquisition, A.W.; investigation, E.G., R.G., N.A.D., O.I.D., M.P.A., J.S.M.S., C.L., M.T. and A.W.; methodology, E.G. and R.G.; project administration, A.W.; supervision, R.G. and A.W.; visualization, E.G. and R.G.; writing—original draft, E.G. and R.G.; writing—review and editing, N.A.D., O.I.D., M.P.A., J.S.M.S., C.L., M.T. and A.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Polish National Science Centre in Cracow, grant preludium NCN 2016/23/NZ8/02796. This study was also supported by the European Commission under the Horizon 2020 Research and Innovation Program GHaNA (The Genus Haslea, New marine resources for blue biotechnology and aquaculture, grant agreement No (734708/GHANA/H2020-MSCA-RISE-2016) J.-L.M.), and also the 2017–2022 research funds granted for implementation of a co-financed international research project from the Polish Ministry of Science and Higher Education.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Molecular data have all been deposited to GenBank. Data are also available on Zenodo with the following link: https://doi.org/10.5281/zenodo.5361687 (accessed on 1 September 2021).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Grunow, A. Diatomeen auf Sargassum von Honduras, gesammelt von Linding. Nova Hedwigia 1867, 6, 1–37. [Google Scholar]
  2. Ross, R. The diatom genus Capartogramma and the identity of Schizostauron. Bull. Br. Mus. Nat. Hist. Bot. 1963, 3, 49–92. [Google Scholar]
  3. Riaux-Gobin, C.; Compére, P.; Hinz, F.; Ector, L. Achnanthes citronella, A. trachyderma comb. nov. Bacillariophyta) and allied taxa pertaining to the same morphological group. Phytotaxa 2015, 227, 101–119. [Google Scholar] [CrossRef] [Green Version]
  4. Davidovich, N.A.; Davidovich, O.I.; Witkowski, A.; Li, C.L.; Dąbek, P.; Mann, D.G.; Zgłobicka, I.; Kurzydłowski, K.J.; Gusev, E.S.; Górecka, E.; et al. Sexual reproduction in Schizostauron (Bacillariophyta) and a preliminary phylogeny of the genus. Phycologia 2017, 56, 77–93. [Google Scholar] [CrossRef]
  5. Górecka, E.; Ashworth, M.P.; Davidovich, N.; Davidovich, O.; Dąbek, P.; Sabir, J.S.; Witkowski, A. Multigene phylogenetic data place monoraphid diatoms Schizostauron and Astartiella along with other fistula bearing genera in the Stauroneidaceae. J. Phycol. 2021, 57, 1472–1491, online ahead of print. [Google Scholar] [CrossRef]
  6. Schütt, F. Bacillariales. In Die Natürlichen Pflanzenfamilien, 1(1b); Engler, A., Prantl, K., Eds.; W. Englemann: Leipzig, Germany, 1896; pp. 31–153. [Google Scholar]
  7. Hustedt, F. Bacillariophyta (Diatomeae). In Die Sübwasser-Flora Mitteleuropas, Zweite Auflage. Heft 10; Pascher, A., Ed.; Gustav Fischer: Jena, Germany, 1930; pp. 1–466. [Google Scholar]
  8. Round, F.E.; Crawford, R.M.; Mann, D.G. The Diatoms. Biology and Morphology of the Genera; Cambridge University Press: Cambridge, UK, 1990; pp. 1–747. [Google Scholar]
  9. Williams, D.; Kociolek, J.P. An Overview of Diatom Classification with Some Prospects for the Future. In The Diatom World; Seckbach, J., Kociolek, J.P., Eds.; Springer: Dordrecht, The Netherlands, 2011; pp. 47–91. [Google Scholar]
  10. Round, F.E.; Bukhtiyarova, L. Revision of Achnanthes sensu lato section Marginulatae Buht. sect. nov. of Achnanthidium Kutz. Diatom Res. 1996, 11, 1–30. [Google Scholar]
  11. Round, F.E.; Bukhtiyarova, L. Four new genera based on Achnanthes (Achnanthidium) together with a re-definition of Achnanthidium. Diatom Res. 1996, 11, 345–361. [Google Scholar] [CrossRef]
  12. Round, F.E.; Basson, P.W. A new monoraphid diatom genus (Pogoneis) from Bahrain and the transfer of previously described species A. hungarica & A. taeniata to new genera. Diatom Res. 1997, 12, 71–81. [Google Scholar]
  13. De Stefano, M.; Marino, D. Morphology and taxonomy of Amphicocconeis gen. nov. (Achnanthales, Bacillariophyceae, Bacillariophyta) with considerations on its relationship to other monoraphid diatom genera. Eur. J. Phycol. 2003, 38, 361–370. [Google Scholar] [CrossRef]
  14. Riaux-Gobin, C.; Witkowski, A.; Ruppel, M. Scalariella a new genus of monoraphid diatom (Bacillariophyta) with a bipolar distribution. Fottea 2012, 12, 13–25. [Google Scholar] [CrossRef] [Green Version]
  15. Kulikovskiy, M.; Lange-Bertalot, H.; Witkowski, A. Gliwiczia gen. nov., a new achnanthoid diatom genus with description of four species new for science. Phytotaxa 2013, 109, 1–16. [Google Scholar] [CrossRef]
  16. Desrosiers, C.; Witkowski, A.; Riaux-Gobin, C.; Zglobicka, I.; Kurzydlowski, K.J.; Eulin, A.; Leflaive, J.; Ten-Hage, L. Madinithidium gen. nov. (Bacillariophyceae), a new monoraphid diatom genus from the tropical marine coastal zone. Phycologia 2014, 53, 583–592. [Google Scholar] [CrossRef]
  17. Kulikovskiy, M.; Maltsev, Y.; Andreeva, S.; Glushchenko, A.; Gusev, E.; Podunay, Y.; Ludwig, T.V.; Tusset, E.; Kociolek, J.P. Description of a new diatom genus Dorofeyukea gen. nov. with remarks on phylogeny of the family Stauroneidaceae. J. Phycol. 2019, 55, 173–185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Witkowski, A.; Li, C.; Zgłobicka, I.; Yu, S.X.; Ashworth, M.; Dąbek, P.; Qin, S.; Tang, C.; Krzywda, M.; Ruppel, M.; et al. Multigene assessment of biodiversity of diatom (Bacillariophyceae) assemblages from the littoral zone of the Bohai and Yellow Seas in Yantai Region of Northeast China with some remarks on ubiquitous taxa. J. Coast. Res. 2016, 74, 166–195. [Google Scholar] [CrossRef] [Green Version]
  19. Gastineau, R.; Kim, S.Y.; Lemieux, C.; Turmel, M.; Witkowski, A.; Park, J.G.; Kim, B.S.; Mann, D.G.; Theriot, E.C. Complete mitochondrial genome of a rare diatom (Bacillariophyta) Proschkinia and its phylogenetic and taxonomic implications. Mitochondrial DNA Part B Resour. 2019, 4, 25–26. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Majewska, R.; Bosak, S.; Frankovich, T.A.; Ashworth, M.P.; Sullivan, M.J.; Robinson, N.J.; Lazo-Wasem, E.A.; Pinou, T.; Nel, R.; Manning, S.R.; et al. Six new epibiotic Proschkinia (Bacillariophyta) species and new insights into the genus phylogeny. Eur. J. Phycol. 2019, 54, 609–631. [Google Scholar] [CrossRef]
  21. Kim, S.Y.; Witkowski, A.; Park, J.G.; Gastineau, R.; Ashworth, M.P.; Kim, B.S.; Mann, D.G.; Li, C.L.; Igersheim, A.; Płociński, T.; et al. The taxonomy and diversity of Proschkinia (Bacillariophyta), a common but enigmatic genus from marine coasts. J. Phycol. 2020, 56, 953–978. [Google Scholar] [CrossRef]
  22. Kulikovskiy, M.S.; Andreeva, S.A.; Gusev, E.S.; Kuznetsova, I.V.; Annenkova, N.V. Molecular phylogeny of monoraphid diatoms and raphe significance in evolution and taxonomy. Biol. Bull. 2016, 43, 398–407. [Google Scholar] [CrossRef]
  23. Ashworth, M.P.; Lobbann, C.S.; Witkowski, A.; Theriot, E.C.; Sabir, M.J.; Baeshen, M.N.; Hajarah, N.H.; Baeshen, N.A.; Sabir, J.S.; Jansen, R.K. Molecular and Morphological Investigations of the Stauros-bearing, Raphid Pennate Diatoms (Bacillariophyceae): Craspedostauros E.J. Cox, and Staurotropis T.B.B. Paddock, and their Relationship to the Rest of the Mastogloiales. Protist 2017, 168, 48–70. [Google Scholar] [CrossRef] [PubMed]
  24. Riaux-Gobin, C.; Saenz-Agudelo, P.; Górecka, E.; Witkowski, A.; Daniszewska-Kowalczyk, G.; Ector, L. Cocconeis vaiamanuensis sp. nov. (Bacillariophyceae) from Raivavae (South Pacific) and allied taxa: Ultrastructural specificities and remarks about the polyphyletic genus Cocconeis Ehrenberg. Mar. Biodivers. 2021, 51, 1–23. [Google Scholar] [CrossRef]
  25. Pogoda, C.S.; Keepers, K.G.; Hamsher, S.E.; Stepanek, J.G.; Kane, N.C.; Kociolek, J.P. Comparative analysis of the mitochondrial genomes of six newly sequenced diatoms reveals group II introns in the barcoding region of cox1. Mitochondrial DNA Part A 2018, 30, 43–51. [Google Scholar] [CrossRef]
  26. Gastineau, R.; Hansen, G.; Poulin, M.; Lemieux, C.; Turmel, M.; Bardeau, J.-F.; Leignel, V.; Hardivillier, Y.; Morançais, M.; Fleurence, J.; et al. Haslea silbo, A Novel Cosmopolitan Species of Blue Diatoms. Biology 2021, 10, 328. [Google Scholar] [CrossRef]
  27. Li, C.; Gastineau, R.; Turmel, M.; Witkowski, A.; Otis, C.; Car, A.; Lemieux, C. Complete chloroplast genome of the tiny marine diatom Nanofrustulum shiloi (Bacillariophyta) from the Adriatic Sea. Mitochondrial DNA Part B 2019, 4, 3374–3376. [Google Scholar] [CrossRef] [Green Version]
  28. Hamsher, S.E.; Keepers, K.G.; Pogoda, C.S.; Stepanek, J.G.; Kane, N.C.; Kociolek, J.P. Extensive chloroplast genome rearrangement amongst three closely related Halamphora spp. (Bacillariophyceae), and evidence for rapid evolution as compared to land plants. PLoS ONE 2019, 14, e0217824. [Google Scholar] [CrossRef] [Green Version]
  29. Lucas, P.; Otis, C.; Mercier, J.P.; Turmel, M.; Lemieux, C. Rapid evolution of the DNA-binding site in LAGLIDADG homing endonucleases. Nucleic Acids Res. 2001, 29, 960–969. [Google Scholar] [CrossRef]
  30. Turmel, M.; Lemieux, C. Evolution of the Plastid Genome in Green Algae. Adv. Bot. Res. 2018, 85, 157–193. [Google Scholar]
  31. Yu, M.; Ashworth, M.P.; Hajrah, N.H.; Khiyami, M.A.; Sabir, M.J.; Alhebshi, A.M.; Al-Malki, A.L.; Sabir, J.S.M.; Theriot, E.C.; Jansen, R.K. Evolution of the plastid genomes in diatoms. Adv. Bot. Res. 2018, 85, 129–155. [Google Scholar]
  32. Gastineau, R.; Davidovich, N.A.; Davidovich, O.I.; Lemieux, C.; Turmel, M.; Wróbel, R.J.; Witkowski, A. Extreme Enlargement of the Inverted Repeat Region in the Plastid Genomes of Diatoms from the Genus Climaconeis. Int. J. Mol. Sci. 2021, 22, 7155. [Google Scholar] [CrossRef] [PubMed]
  33. Brembu, T.; Winge, P.; Tooming-Klunderud, A.; Nederbragt, A.J.; Jakobsen, K.S.; Bones, A.M. The chloroplast genome of the diatom Seminavis robusta: New features introduced through multiple mechanisms of horizontal gene transfer. Mar. Genom. 2014, 16, 17–27. [Google Scholar] [CrossRef]
  34. Gastineau, R.; Hamedi, C.; Baba Hamed, M.B.; Abi-Ayad, S.-M.E.-A.; Bąk, M.; Lemieux, C.; Turmel, M.; Dobosz, S.; Wróbel, R.J.; Kierzek, A.; et al. Morphological and molecular identification reveals that waters from an isolated oasis in Tamanrasset (extreme South of Algerian Sahara) are colonized by opportunistic and pollution-tolerant diatom species. Ecol. Ind. 2021, 121, 107104. [Google Scholar] [CrossRef]
  35. Andersen, R.A.; Kawachi, M. Traditional microalgae isolation techniques. In Algal Culturing Techniques; Andersen, R.A., Ed.; Elsevier: London, UK, 2005; pp. 83–100. [Google Scholar]
  36. Guillard, R.R.L. Culture of phytoplankton for feeding marine invertebrates. In Culture of Marine Invertebrate Animals; Smith, W.L., Chanley, M.H., Eds.; Plenum Press: New York, NY, USA, 1975; pp. 29–60. [Google Scholar]
  37. Doyle, J.J.; Doyle, J.L. Isolation of plant DNA from fresh tissue. Focus 1990, 12, 13–15. [Google Scholar]
  38. Bankevich, A.; Nurk, S.; Antipov, D.; Gurevich, A.A.; Dvorkin, M.; Kulikov, A.S.; Lesin, V.M.; Nikolenko, S.I.; Pham, S.; Prjibelski, A.D.; et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012, 19, 455–477. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Gordon, D.; Green, P. Consed: A graphical editor for next-generation sequencing. Bioinformatics 2013, 29, 2936–2937. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  40. Turmel, M.; Otis, C.; Lemieux, C. Divergent copies of the large inverted repeat in the chloroplast genomes of ulvophycean green algae. Sci. Rep. 2017, 7, 994. [Google Scholar] [CrossRef] [Green Version]
  41. Greiner, S.; Lehwark, P.; Bock, R. OrganellarGenomeDRAW (OGDRAW) version 1.3.1: Expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res. 2019, 47, W59–W64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Darling, A.E.; Mau, B.; Perna, N.T. progressiveMauve: Multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 2010, 5, e11147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Crooks, G.E.; Hon, G.; Chandonia, J.-M.; Brenner, S.E. WebLogo: A sequence logo generator. Genome Res. 2004, 14, 1188–1190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Stamatakis, A. RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014, 30, 1312–1313. [Google Scholar] [CrossRef]
  45. Katoh, K.; Standley, D.M. A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinformatics 2016, 32, 1933–1942. [Google Scholar] [CrossRef]
  46. Capella-Gutiérrez, S.; Silla-Martínez, J.M.; Gabaldón, T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009, 25, 1972–1973. [Google Scholar] [CrossRef]
  47. Darriba, D.; Taboada, G.L.; Doallo, R.; Posada, D. jModelTest 2: More models, new heuristics and parallel computing. Nature Met. 2012, 9, 772. [Google Scholar] [CrossRef] [Green Version]
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Figure 1. Light (LM) and Scanning electron microscopy (SEM) images of S. trachyderma. (a–c): live specimen with plastids. (a,b): valve view. (c): girdle view. (d–g): in LM. (d,e): raphe valve. (f–g): sternum valve. (h–k): in SEM. (h): sternum valve. (i): raphe valve.
Figure 1. Light (LM) and Scanning electron microscopy (SEM) images of S. trachyderma. (a–c): live specimen with plastids. (a,b): valve view. (c): girdle view. (d–g): in LM. (d,e): raphe valve. (f–g): sternum valve. (h–k): in SEM. (h): sternum valve. (i): raphe valve.
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Figure 2. Map of the mitochondrial genome of S. trachyderma.
Figure 2. Map of the mitochondrial genome of S. trachyderma.
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Figure 3. MAUVE alignment of the mitochondrial genomes of Berkeleya fennica (KM886611), Didymosphenia geminata (KX889125), Fistulifera saprophila (MT383640), Fistulifera solaris (KT363689), Proschkinia sp. (MH800316), and Schizostauron trachyderma (MZ520767). The legend below shows the gene content of the blocks of synteny (conserved protein-coding genes and rRNA only).
Figure 3. MAUVE alignment of the mitochondrial genomes of Berkeleya fennica (KM886611), Didymosphenia geminata (KX889125), Fistulifera saprophila (MT383640), Fistulifera solaris (KT363689), Proschkinia sp. (MH800316), and Schizostauron trachyderma (MZ520767). The legend below shows the gene content of the blocks of synteny (conserved protein-coding genes and rRNA only).
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Figure 4. Map of the plastid genome of S. trachyderma.
Figure 4. Map of the plastid genome of S. trachyderma.
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Figure 5. Sequence motifs obtained by aligning LAGLIDADG proteins from Schizostauron trachyderma and 13 sequences from various species of Chlorophyceae corresponding to IB4-L8 LAGLIDADG proteins. The alignment displayed as a LOGO shows the presence of two conserved motifs, QWIVGFVDG and PFFE.
Figure 5. Sequence motifs obtained by aligning LAGLIDADG proteins from Schizostauron trachyderma and 13 sequences from various species of Chlorophyceae corresponding to IB4-L8 LAGLIDADG proteins. The alignment displayed as a LOGO shows the presence of two conserved motifs, QWIVGFVDG and PFFE.
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Figure 6. Comparison of the gene composition for the plastid genomes of all the species used in the phylogeny below. A 1/blue indicates the presence of the gene, a 0/white its lack, and a Ψ/green a pseudogene version of the gene.
Figure 6. Comparison of the gene composition for the plastid genomes of all the species used in the phylogeny below. A 1/blue indicates the presence of the gene, a 0/white its lack, and a Ψ/green a pseudogene version of the gene.
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Figure 7. Maximum likelihood phylogeny inferred from an alignment of concatenated protein-coding genes from 37 mitochondrial genomes of diatoms, including that of S. trachyderma. The araphid species Ulnaria acus served as an outgroup in this analysis. The best scoring RAxML tree (log likelihood = −414,469.369802) is presented with bootstrap support values denoted on the nodes. The scale bar indicates the number of substitutions per site. The araphid species Ulnaria acus is used as an outgroup.
Figure 7. Maximum likelihood phylogeny inferred from an alignment of concatenated protein-coding genes from 37 mitochondrial genomes of diatoms, including that of S. trachyderma. The araphid species Ulnaria acus served as an outgroup in this analysis. The best scoring RAxML tree (log likelihood = −414,469.369802) is presented with bootstrap support values denoted on the nodes. The scale bar indicates the number of substitutions per site. The araphid species Ulnaria acus is used as an outgroup.
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Figure 8. Maximum likelihood phylogeny inferred from an alignment of concatenated protein-coding genes from 26 plastid genomes of diatoms, including that of S. trachyderma. The araphid species Ulnaria acus served as an outgroup in this analysis. The best scoring RAxML tree (log likelihood = −878,702.878358) is presented with bootstrap support values denoted on the nodes. The scale bar indicates the number of substitutions per site.
Figure 8. Maximum likelihood phylogeny inferred from an alignment of concatenated protein-coding genes from 26 plastid genomes of diatoms, including that of S. trachyderma. The araphid species Ulnaria acus served as an outgroup in this analysis. The best scoring RAxML tree (log likelihood = −878,702.878358) is presented with bootstrap support values denoted on the nodes. The scale bar indicates the number of substitutions per site.
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Table
Table 1. List of the various ORF found in the mitochondrial and plastid genomes of Schizostauron trachyderma, with the name, position, putative conserved domains, and best blastp result.
Table 1. List of the various ORF found in the mitochondrial and plastid genomes of Schizostauron trachyderma, with the name, position, putative conserved domains, and best blastp result.
NamePositionPutative Conserved DomainBest Blastp Result
(E-Value, Identity)
orf143aPlastid genome (LSC)NoneCAA45586.1 from Cylindrotheca closterium (2 × 10−58, 69.23%)
orf227aPlastid genome (LSC)Putative serine recombinaseAZJ16760.1 from Semiavis robusta (9 × 10−128, 85.31%)
orf166aPlastid genome (LSC)NoneAZJ16664.1 from Seminavis robusta (2 × 10−24, 36.88%)
orf123bPlastid genome (LSC)NoneWP_101018572.1 from Olleya sp. (3 × 10−6, 34.29%)
orf148bPlastid genome (LSC)NoneAXF37983.1 from Seminavis robusta (6 × 10−35, 66.41%)
orf406aPlastid genome (LSC)NoneCAA45586.1 from Cylindrotheca closterium (0.0, 91.75%)
orf152bPlastid genome (LSC)NoneYP_009028997.1 from Cylindrotheca closterium (2 × 10−33, 44.30%)
orf418aPlastid genome (LSC)Putative integrase recombinaseYP_009686230.1 from Halamphora calidilacuna (1 × 10−39, 50.00%)
orf175aPlastid genome (LSC)NoneQUW40432.1 from Haslea silbo (5 × 10−21, 33.88%)
orf147aPlastid genome (LSC)NoneNone significant
orf134aPlastid genome (LSC)Putative integrase recombinase (not complete, contains His-289, Arg-292, and Tyr-324)YP_009029005.1 from Cylindrotheca closterium (5 × 10−63, 74.63%)
orf104aPlastid genome (LSC)Putative integrase recombinase (not complete)YP_009686252.1 from Halamphora calidilacuna (2 × 10−27, 56.31%)
orf187bPlastid genome (LSC)NoneHAC63963.1 from Cyanothece sp. (1 × 10−119, 94.59%)
orf110aPlastid genome (LSC)Putative serine recombinase (not complete in C terminal, lacks the DNA binding site)QGW12742.1 from Nanofrustulum shiloi (1 × 10−47, 85.26%)
orf238bPlastid genome (LSC)NoneQUS63763.1 from Haslea silbo (3 × 10−23, 35.02%)
orf417bPlastid genome (LSC)NoneAXF37982.1 from Seminavis robusta (5 × 10−53, 30.82%)
orf224aPlastid genome (LSC)Putative serine recombinaseYP_009496149.1 from Plagiogrammopsis vanheurckii (6 × 10−135, 88.79%)
orf127aPlastid genome (LSC)NoneNone significant
orf103aPlastid genome (LSC)NoneYP_009028999.1 from Cylindrotheca closterium (6 × 10−17, 45.79%)
orf158bPlastid genome (LSC)NoneYP_009029000.1 from Cylindrotheca closterium (4 × 10−25, 52.94%)
orf299aPlastid genome (LSC)Putative integrase recombinaseYP_009497021.1 from Psammoneis obaidii (7 × 10−151, 76.77%)
orf305aPlastid genome (LSC)NoneAZJ16668.1 from Seminavis robusta (2 × 10−154, 74.43%)
orf494aPlastid genome (IR)Putative reverse transcriptaseQGW12739.1 from Nanofrustulum shiloi (0.0, 58.17%)
orf119Plastid genome (IR)Putative serine recombinase (not complete in N terminal, lacks most of the presynaptic site 1 dimer interface)QGW12742.1 from Nanofrustulum shiloi (6 × 10−56, 68.03%)
orf139Plastid genome (IR)Putative LAGLIDADGAAL34315.1 from Pterosperma cristatum (2 × 10−66, 77.34%)
orf100Plastid genome (IR)NoneAZJ16668.1 from Seminavis robusta (5 × 10−9, 68.29%)
orf190aPlastid genome (SSC)NoneYP_009308934.1 from Toxarium undulatum (2 × 10−65, 61.96%)
orf144aPlastid genome (SSC)NoneNone significant
orf132bPlastid genome (SSC)NoneAZJ16659.1 from Seminavis robusta (2 × 10−71, 90.52%)
orf391aPlastid genome (SSC)NoneCAA45582.1 from Cylindrotheca fusiformis (2 × 10−168, 73.63%)
orf112aPlastid genome (SSC)Putative integrase recombinase (not complete in C terminal, displays only the first conserved Arg-173)YP_009028833.1 from Asterionellopsis glacialis (1 × 10−47, 90.00%)
orf117cPlastid genome (SSC)NoneCAA45586.1 from Cylindrotheca closterium (2 × 10−50, 74.77%)
orf152aPlastid genome (SSC)NoneHAC63961.1 from Cyanothece sp. (3 × 10−102, 97.32%)
orf317aPlastid genome (SSC)Putative integrase recombinaseNNF85095.1 from Winogradskyella sp. (4 × 10−88, 53.01%)
orf290bPlastid genome (SSC)NoneYP_009028832.1 from Asterionellopsis glacialis (8 × 10−61, 51.33%)
orf188aPlastid genome (SSC)NoneAZJ16664.1 from Seminavis robusta (3 × 10−93, 76.63%)
orf234aPlastid genome (SSC)Putative serine recombinaseQWM93463.1 from Tryblionella apiculata (1 × 10−140, 88.53%)
orf148aPlastid genome (SSC)NoneYP_009059189.1 from Eunotia naegelii (3 × 10−15, 32.89%)
orf313aPlastid genome (SSC)NoneQUS63950.1 from Haslea silbo (5 × 10−28, 51.55%)
orf120bPlastid genome (SSC)NoneNone significant
orf294aPlastid genome (SSC)Putative integrase recombinaseYP_009495909.1 from Plagiogramma staurophorum (6 × 10−176, 83.33%)
orf516aPlastid genome (SSC)NoneCAA45586.1 from Cylindrotheca closterium (2 × 10−92, 34.58%)
orf645MitogenomePutative reverse transcriptaseYP_009317775.1 from Navicula ramosissima (0.0, 82.20%)
orf690MitogenomePutative reverse transcriptaseQUS63794.1 from Haslea silbo (0.0, 93.14%)
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Górecka, E.; Gastineau, R.; Davidovich, N.A.; Davidovich, O.I.; Ashworth, M.P.; Sabir, J.S.M.; Lemieux, C.; Turmel, M.; Witkowski, A. Mitochondrial and Plastid Genomes of the Monoraphid Diatom Schizostauron trachyderma. Int. J. Mol. Sci. 2021, 22, 11139. https://doi.org/10.3390/ijms222011139

AMA Style

Górecka E, Gastineau R, Davidovich NA, Davidovich OI, Ashworth MP, Sabir JSM, Lemieux C, Turmel M, Witkowski A. Mitochondrial and Plastid Genomes of the Monoraphid Diatom Schizostauron trachyderma. International Journal of Molecular Sciences. 2021; 22(20):11139. https://doi.org/10.3390/ijms222011139

Chicago/Turabian Style

Górecka, Ewa, Romain Gastineau, Nikolai A. Davidovich, Olga I. Davidovich, Matt P. Ashworth, Jamal S. M. Sabir, Claude Lemieux, Monique Turmel, and Andrzej Witkowski. 2021. "Mitochondrial and Plastid Genomes of the Monoraphid Diatom Schizostauron trachyderma" International Journal of Molecular Sciences 22, no. 20: 11139. https://doi.org/10.3390/ijms222011139

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