DeepDyve requires Javascript to function. Please enable Javascript on your browser to continue.
Organellar genomes of giant kelp from the southern hemisphere Organellar genomes of giant kelp from the southern hemisphere
Iha, Cintia; Layton, Cayne; Flentje, Warren; Lenton, Andrew; Johnson, Craig; Fraser, Ceridwen I.; Willis, Anusuya
2023-12-31 00:00:00
British Phycological APPLIED PHYCOLOGY Society 2023, VOL. 4, NO. 1, 78–86 Understanding and using algae https://doi.org/10.1080/26388081.2023.2193619 a,b b c d b e Cintia Iha , Cayne Layton , Warren Flentje , Andrew Lenton , Craig Johnson , Ceridwen I. Fraser and Anusuya Willis a b Australian National Algae Culture Collection ANACC, CSIRO, National Collections and Marine Infrastructure, Hobart, TAS, Australia; Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia; Mineral Resources, CSIRO, Parkville, VIC, Australia; d e Permanent Carbon Locking Future Science Platform, Oceans and Atmosphere, CSIRO, Hobart, TAS, Australia; Department of Marine Science, University of Otago, New Zealand ABSTRACT ARTICLE HISTORY Received 27 August 2022 Macrocystis pyrifera is a foundation species that creates kelp forests and supports essential Accepted 12 March 2023 ecosystem services across coastal environments. Over the past half-century, more than 95% of giant kelp forests have declined around Tasmania and Australia due to climate change, causing KEYWORDS a near-complete loss of the ecosystems and services they support. Compared with northern Chloroplast; genetic hemisphere giant kelp ecosystems, Australian populations have received little research attention diversity; kelp forest; in genomic and other genetic analyses. We present the complete mitochondrial and chloroplast macrocystis pyrifera; genomes of Macrocystis pyrifera from Tasmania. Both organellar genomes were similar to pub- mitochondrion; phylogeny; tasmania lished Laminariales genomes in length, GC content, gene composition and synteny. A phylogeny constructed by combining protein-coding genes from both genomes showed Tasmanian speci- mens clustered with M. pyrifera specimens from the northern hemisphere. Genetic differences in protein genes between the Tasmanian M. pyrifera and the northern hemisphere specimens were overall low, but some ribosomal protein genes presented higher values of nonsynonymous mutations. The most divergent gene, the mitochondrial conserved hypothetical protein ORF377, can provide insights into the evolution of the species. This gene has been proposed as a suitable molecular marker for population genetic research in Fucales and may also be helpful for intraspe- cific studies of M. pyrifera. The complete mitochondrial and chloroplast genomes of Tasmanian M. pyrifera provide important genetic data and critical information for further evolutionary and population studies and for managing these endangered and disappearing populations. Introduction Until recently, the genus Macrocystis was divided into Macrocystis pyrifera (Linnaeus) C.Agardh (Laminariales, four species based mainly on the morphology of the blades Ochrophyta), commonly known as giant kelp, is a rapidly and holdfast. However, the morphological variability is growing foundation species that forms tall kelp forests. probably driven by environmental effects on the early Giant kelp forests support productive and diverse com- development of the sporophytes, and all species have col- munities and provide essential ecosystem services to lapsed into M. pyrifera (Demes, Graham, & Suskiewicz, coastal environments (Schiel & Foster, 2015). Changes 2009). Posterior DNA barcoding studies supported the in regional oceanography and environmental conditions, recognition of a single species (Macaya & Zuccarello, including warming waters and declines in coastal nutri- 2010a). This taxonomic revision turned M. pyrifera into ents, have been associated with ~95% declines in giant the only kelp present in both the northern and southern kelp coverage around Tasmania since 1940s (Butler, hemispheres. In the northern hemisphere, it is present Lucieer, Wotherspoon, & Johnson, 2020; Johnson et al., along the North American west coast, while in the south- 2011). Recently, efforts have been made to restore these ern hemisphere, it is relatively widespread across tempe- disappearing kelp forests in Tasmania, using selective rate and sub-Antarctic coasts (Graham, Vasquez, & breeding and seeding populations from remnant loca- Buschmann, 2007; Mora‐soto et al., 2021). Although tions (Layton & Johnson, 2021; Layton et al., 2020). there is a broader distribution of M. pyrifera across the Despite the importance of M. pyrifera in Tasmania, southern hemisphere, there is only information on mito- there is limited genomic information to represent the chondrial and chloroplast genomes from individuals from species from the southern hemisphere. the northern hemisphere. Overall, there have been few CONTACT Cintia Iha cintiaiha@gmail.com Supplemental data for this article can be accessed online at https://doi.org/10.1080/26388081.2023.2193619. © 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the posting of the Accepted Manuscript in a repository by the author(s) or with their consent. APPLIED PHYCOLOGY 79 genetic studies surveying giant kelp populations from the Trimmomatic 0.38 (Bolger, Lohse, & Usadel, 2014) southern hemisphere, and these were based on a few mole- using the parameter SLIDINGWINDOW:4:20 cular markers or microsatellites (Astorga, Hernández, HEADCROP:14 MINLEN:120. We performed an initial Valenzuela, Avaria-Llautureo, & Westermeier, 2012; genome assembly with SPAdes v. 3.15.3 (Prjibelski, Camus, Faugeron, & Buschmann, 2018; Coyer, Smith, & Antipov, Meleshko, Lapidus, & Korobeynikov, 2020), Andersen, 2001; Durrant, Barrett, Edgar, Coleman, & setting different k-mer sizes (−k) 21,33,55 and isolate Burridge, 2015; Macaya & Zuccarello, 2010a, 2010b). flags (–isolate). We identified the mitochondrian and These molecular markers, especially the organellar genes chloroplast contigs using BLASTn search against pub- cox1 and rbcL, showed a low divergence between giant kelp lished M. pyrifera genomes (mitochondrion: populations (Durrant, Barrett, Edgar, Coleman, & MH411105; chloroplast: MZ156032). The SPAdes assem- Burridge, 2015). Mitochondria and chloroplast genomes bly did not recover the entire genomes. We performed provide greater insight into evolutionary questions and can another assembly with NOVOplasty (Dierckxsens, generate robust phylogenies (Iha et al., 2018). These data Mardulyn, & Smits, 2016) using as a seed the longest may also be helpful in finding more suitable molecular SPAdes contig for each genome, which recovered both markers for genetic population analyses. Therefore, here completed and circular genomes. We checked the assem- we present the full mitochondrial and chloroplast genomes blies by mapping the reads against the genomes using of Macrocystis pyrifera from Tasmania to increase our Bowtie2 v.2.4.4 (Langmead & Salzberg, 2012). Both mito- understanding of the differences between organellar gen- chondrial and chloroplast genomes were annotated using omes from northern and southern hemisphere popula- MFannot (https://megasun.bch.umontreal.ca/cgi-bin tions and to facilitate future research. /mfannot/mfannotInterface.pl), RNAweasel (https:// megasun.bch.umontreal.ca/cgi-bin/RNAweasel/ RNAweaselInterface.pl) and ARAGORN (http://www. Material and methods ansikte.se/ARAGORN/). The automatic organellar gen- ome tools above did not recover the ribosomal 5S RNA Collection, DNA extraction and sequencing for the chloroplast genome, and we searched for this gene To obtain the organellar genomes, we collected approxi- in the 5SrRNAdb (http://combio.pl/rrna; Szymanski, mately 30 cm of the apical lamina from an adult M. Zielezinski, Barciszewski, Erdmann, & Karlowski, 2016). pyrifera sporophyte at Blackmans Bay, Tasmania, Australia (43°01’02.4“S, 147°19’45.8“E). The tissue was Phylogenetic and genomic analysis rinsed in deionized water and dried on absorbent paper. Small samples, ~3 cm , were cut from the thinnest por- To perform the phylogenetic analyses, we selected 12 tions of the lamina and stored in silica gel. Qiagen Laminariales species available in GenBank for each DNeasy PowerPlant Pro Kit was used for DNA extrac- mitochondrial and chloroplast genome tion, following the modified method outlined by Peters, (Supplementary Table S1). We extracted the coding Waters, Dutoit, and Fraser (2020). Samples were soaked genes from each genome in Geneious Prime® v2022.1.1 for 24 h at 65°C in 500 µl of PowerBead solution and 3 µl (Biomatters, Auckland, New Zealand), which were of RNase A. After incubation, 100 µl of isopropanol was translated to protein sequences with SeqKit v2.1.0 added and incubated at 65°C for 90 min, with vortexing (Shen, Le, Li, Hu, & Zou, 2016) using the subcommand every 30 min. Samples were then placed in a FASTPREP- “translate” and setting the genetic code standard (1) for 24™ 5 G homogenizer (MP Biomedicals, Santa Ana, mitochondrial genes and bacterial code (11) for chlor- California, USA) for 40 s. Subsequent steps followed the oplast genes. For each protein, we created a matrix manufacturer’s protocols, with elution of DNA in 100 µl aligning the amino acid sequences with MUSCLE of TE buffer, incubated for 10 min before centrifugation. v5.0.1430 (Edgar, 2004). We concatenated all mitochon- The DNA library and whole-genome sequencing were drial and chloroplast protein matrixes to generate carried out by the Australian Genome Research Facility a supermatrix using FASconCAT-G script (https:// (Melbourne, Australia). Sequencing was performed on github.com/PatrickKueck/FASconCAT-G). The phylo- Illumina NovaSeq 500 using PE 150 bp High Output kit geny was constructed with IQtree 2.0.7 (Minh et al., (Illumina, San Diego, California, USA). 2020). ModelFinder (Kalyaanamoorthy, Minh, Wong, von Haeseler, & Jermiin, 2017) was used to select the best-fit model for each gene, with 1000 ultrafast boot- Genome assembly and annotation strap replicates (Hoang, Chernomor, von Haeseler, Read quality was checked using FASTQC v.0.11.8 Minh, & Vinh, 2018) and with Chorda asiatica Sasaki (Andrews, 2010), and pair reads were trimmed using & Kawai, Pseudochorda nagaii (Tokida) Inagaki and 80 C. IHA ET AL. Akkesiphycus lubricus Yamada & Tanaka as outgroups. genome (Fig 1) was 37,326 bp and had 31.8% GC con- We also constructed phylogenies for each organelle tent. The gene content was 37 protein-coding genes, using the same approach described above. including two widely conserved open reading frame There was one mitochondrial and chloroplast gen- (ORF) genes, three ribosomals (LSU, SSU and 5S ome, each of M. pyrifera from the northern hemisphere, rRNA) and 25 transfer RNA genes. None of the genes was available in GenBank at the time of the develop- was found to contain introns. The chloroplast genome ment of this research. We used these genomes to per- (Fig 2) was 130,201 bp long and had 30.9% GC content. form comparative genomic analysis and calculate It contained 142 protein-coding genes, including three evolutionary rates for protein-coding genes. For the widely conserved ORF genes, 28 tRNAs and two copies chloroplast genome (accession number: MZ156032), of LSU, SSU and 5S ribosomal RNAs situated in dupli- we used a specimen from British Columbia, Canada cated and reversed regions. The tRNA for leucine (Starko et al., 2021). The currently available (tRNA-Leu) contains a group I intron, which is con- M. pyrifera mitochondria genome (accession number: served in Laminariales plastomes (Starko et al., 2021). MH411105) belongs to a specimen from Perharidy, Our phylogenetic analysis aimed to put the France (Chen, Zang, Shang, & Tang, 2019). While the Tasmanian M. pyrifera in a phylogenetic context. As original population of that specimen is unclear because expected, Tasmanian M. pyrifera clustered with north- M. pyrifera is not naturally found in Europe, and those ern hemisphere specimens in the combined mitochon- individuals were introduced to the Brittany coast in drial and chloroplast phylogeny (Fig 3a). The France in the early 1970s, they probably phylogenetic reconstruction was strongly resolved, originated from California (Boalch, 1981). We recon- almost all congruent with the prior Laminariales phylo- structed a haplotype network for the cytochrome geny based on combined chloroplast, mitochondrial c oxidase subunit I gene (cox1) to investigate the origin and ribosomal genes (Starko et al., 2019). The incon- of M. pyrifera in France. We extracted the partial cox1 gruence is found within the Araliaceae family, repre- sequence from the mitochondrial genome of the French sented here with Undaria pinnatifida (Harvey) specimen and aligned it with cox1 sequences obtained Suringar, Alaria crispa Kjellman, Lessoniopsis litoralis by Macaya and Zuccarello (2010a) and Durrant, Barrett, (Tilden) Reinke and Pterygophora californica Ruprecht. Edgar, Coleman, and Burridge (2015). The reconstruc- Alaria crispa clustered with a low-supported clade tion was performed with the minimum spanning formed by Lessoniopsis littoralis and Pterygophora cali- method using PopART v.17 (Leigh, Bryant, Nakagawa, fornica in our tree (Fig 3a), while the Alaria genus was & Nakagawa, 2015). close to Undaria pinnatifida in the previous phyloge- The genomic architecture was compared using the netic reconstruction (Starko et al., 2019). The chloro- MAUVE plugin in Geneious Primer. We calculated plast phylogeny was similar to the combined the pairwise divergence, synonymous substitution phylogenetic tree, while the internal branching in the (dS) and nonsynonymous substitution (dN) rates for Araliaceae clade was not supported in the mitochondrial each coding gene between the Tasmanian M. pyrifera tree (Fig S1). Conflicting evolutionary history between and the northern hemisphere specimens. We aligned mitochondrial and chloroplast phylogenies of brown the genes at the codon level with PRANK v.170427 algae and other algal lineages is common, and chloro- (Löytynoja, 2014). The uncorrected pairwise distances plast phylogenies have been shown to be more powerful were calculated with mothur 1.46.1 (Schloss et al., in constructing better-resolved phylogenies (Lyra et al., 2009) using “dist.seqs” command. dN and dS rates 2021; Starko et al., 2019). Understanding the evolution- were calculated using CODEML command from ary factors that may cause phylogenetic incongruencies PAML v4.9 (Yang, 2007), setting the runmode as is beyond the scope of this study. “pairwise”. Plots were constructed using ggplot2 Our haplotype network analysis strongly indicates v3.3.5 (Wickham, 2016). that the French M. pyrifera was originally from the northeast Pacific (Fig 3b). The partial cox1 sequence from the French specimen is identical to the haplotype Results and discussion 2 (H2) that shared sequences with samples from California and Canada (Macaya & Zuccarello, 2010a). The mitochondrial (Fig 1; GenBank accession: The haplotype from the Tasmanian M. pyrifera speci- ON227496) and chloroplast (Fig 2; GenBank accession: men is identical to previous sequences obtained from ON227495) genomes were similar to published the southern part of Australia, including Tasmania Laminariales genomes in length, GC and gene content (Durrant, Barrett, Edgar, Coleman, & Burridge, 2015), (Starko et al., 2021). The length of the mitochondrial APPLIED PHYCOLOGY 81 Figure 1. Mitochondrial genome map. and New Zealand, located in haplotype 1 (H1) (Fig 3b; Supplementary Table S2). Previous studies have demon- Macaya & Zuccarello, 2010a). strated that the genetic diversity in mitochondrial The gene composition and synteny between sequences of M. pyrifera worldwide is low (Macaya & Tasmanian and northern hemisphere specimens for Zuccarello, 2010a, 2010b) and that plastid sequences either organelle genome showed no difference, and the have lower diversity than mitochondrial ones nucleotide composition was very similar throughout the (Durrant, Barrett, Edgar, Coleman, & Burridge, 2015). genome (Fig 3c). Considering only coding genes (pro- The same was observed with synonymous (dS) and non- teins), the divergences were also low (Fig 4a), but mito- synonymous (dN) substitution rates, which were low chondrial protein genes presented higher pairwise compared to organelle genes from northern hemisphere divergence, 1.14% on average, compared to chloroplast and Tasmanian M. pyrifera (Fig 4b,c), and mitochon- genes, with 0.15% on average (Fig 4a, Table 1, drial rates were higher than chloroplast rates. Almost 82 C. IHA ET AL. Figure 2. Chloroplast genome map. half of the plastid genes (67) did not show any diver- M. pyrifera originated from the northern hemisphere gence, and from the 74 genes where divergence was coast and experienced a recent dispersal to the southern present, only 40 showed a non-synonymous mutation hemisphere (Coyer, Smith, & Andersen, 2001; Estes & (Supplementary Table S2). This general low genetic Steinberg, 1988; Macaya & Zuccarello, 2010a). diversity may indicate that mitochondrial and plastid Although the comparison between northern hemi- genomes are under strong constraint (Starko et al., sphere M. pyrifera with Tasmanian specimens’ genomes 2021) even between populations separated by the furth- does not show high differences, complete organellar gen- est geographic distances. It has been postulated that omes can give insights into this species’ evolution and APPLIED PHYCOLOGY 83 Figure 3. (a) Maximum likelihood phylogeny combining concatenated coding sequences from mitochondria and chloroplasts. Ultrafast bootstrapping is shown in the support values, only above 90%. (b) Haplotype network for cox1 from Macrocystis pyrifera. Haplotypes were obtained from Macaya et al. (2010) and Durrant, Barrett, Edgar, Coleman, and Burridge (2015), in which each haplotype represented only one sequence. Mutations are shown as hatch marks in connecting lines. Haplotypes are shaded according to geographic origin. (c) Whole-genome alignment built with MAUVE. Locally Collinear Blocks (LCBs; light red) show high similarities between genomes from southern and northern hemisphere individuals. Below LCB, gene synteny of each genome is shown: ribosomal RNA genes in red, coding genes in white and transfer RNA genes in green. Orange blocks in chloroplast genomes indicate repeat regions. provide useful data for studying the evolution of other Laminariales, as its orthologue is present in all mitochon- brown algae. Most of the genes that had the highest dN drial genomes from Laminariales sequenced so far. This values (Table 1) are ribosomal proteins (rpl or rps), espe- region has been considered a strong candidate for genetic cially in the mitochondrian. Ribosomal proteins are population studies in Fucales (Graf et al., 2017). Although responsible for ribosome biogenesis and are crucial for this locus is potential to population studies in protein synthesis. Non-synonymous mutation would Laminariales, this gene is not widespread in indicate a response to local adaptation. However, the Phaeophyceae. For example, it is absent in the mitochon- effect of these mutations on those genes is unknown, drial genomes of Ectocarpus (Cock et al., 2010), Pylaiella and further research should be conducted to understand (Oudot-Le Secq, Fontaine, Rousvoal, Kloareg, & whether the nonsynonymous mutations are indeed Loiseaux-De Goer, 2001), Analipus (Starko et al., 2021) related to the adaptation in different locations. The most and Dictyota (Oudot-Le Secq, Loiseaux-de Goer, Stam, & divergent gene found among both mitochondrial and Olsen, 2006). chloroplast genes is the conserved hypothetical protein Here, we provide novel and important genetic ORF377 (Table 1), located between cox3 and atp6 data for populations that may be on the verge of (Fig 1) in the mitochondrial genome. It also presented extinction – the giant kelp forests of southern the highest dN value. The gene function is unknown and Australia. These new organellar genomes of does not present known conserved domains. Its higher a southern hemisphere M. pyrifera specimen are divergence indicates that this gene may be a potential essential for future genetic and evolutionary studies. marker for genetic studies in M. pyrifera and other Many genetic studies have used organellar markers 84 C. IHA ET AL. Figure 4. Genetic variation distribution of chloroplast and mitochondrial coding proteins. (a) uncorrected pairwise divergence, (b) synonymous substitution rate and (c) nonsynonymous substitution rate. Table 1. The top 10 protein genes with the highest nonsynonymous substitution rates in chloroplast and mitochondrial genomes. dN, nonsynonymous substitution rates; dS, synon- ymous substitution rates. Gene Sequence Length Pairwise Divergence dN dS Chloroplast ycf34 285 1.06% 0.0119 1.00E–04 rpl32 237 0.85% 0.0105 1.00E–04 orf147 441 0.45% 0.0073 1.00E–04 rpl5 561 0.36% 0.0043 0 rpl4 645 0.31% 0.0038 0 ycf19 357 0.28% 0.0037 0 rpl1 690 0.29% 0.0036 0 ycf54 372 0.27% 0.0031 0 atpG 468 0.43% 0.0029 0.0092 rpl9 465 0.43% 0.0029 0.0115 Mitochondrion orf377 1131 4.07% 0.0357 0.1047 rpl31 204 2.46% 0.0179 0.0628 rps11 495 2.23% 0.0119 0.1181 rps7 495 1.42% 0.0097 0.0486 rps12 390 2.09% 0.0096 0.0821 rps2 648 1.08% 0.0093 0.0224 cox2 3852 1.33% 0.0079 0.048 rps4 795 0.88% 0.0072 0.026 rps8 369 1.63% 0.0067 0.0719 tatC 750 1.60% 0.0052 0.0683 with low genetic variation, such as cox1 and rbcL, Funding that possibly hide the real genetic structure of this This work was funded by CSIRO through the Permanent species. Our results identified a region in the mito- Carbon Locking Future Science Platform and the Towards chondrial genome that may be developed for future Net Zero Mission; CIF was supported by a Rutherford rapid genetic surveys, which may be valuable for the Discovery Fellowship from the Royal Society of New Zealand under Grant RDF-UOO1803; CL receives funding management of these endangered and disappearing from The Nature Conservancy, California Oceans Program. M. pyrifera populations. Disclosure statement ORCID No potential conflict of interest was reported by the authors. Cintia Iha http://orcid.org/0000-0003-4420-5131 APPLIED PHYCOLOGY 85 Cock, J. M., Sterck, L., Rouze, P., Scornet, D., Allen, A. E., Cayne Layton http://orcid.org/0000-0002-3390-6437 Andrew Lenton http://orcid.org/0000-0001-9437-8896 Amoutzias, G., Anthouard, V., Artiguenave, F., Aury, J. M., Craig Johnson http://orcid.org/0000-0002-9511-905X Badger, J. H., Beszteri, B et al. (2010). The Ectocarpus Ceridwen I. Fraser http://orcid.org/0000-0002-6918-8959 genome and the independent evolution of multicellularity Anusuya Willis http://orcid.org/0000-0003-0829-7446 in brown algae. Nature, 465, 617–621. doi:10.1038/ nature09016 Coyer, J. A., Smith, G. J., & Andersen, R. A. (2001). EVOLUTION of Macrocystis SPP. (PHAEOPHYCEAE) as Data availability statement DETERMINED by ITS1 and ITS2 SEQUENCES1. Journal The data that support the findings of this study are openly of Phycology, 37, 574–585. doi:10.1046/j.1529-8817.2001. available in GenBank (https://www.ncbi.nlm.nih.gov/gen 037001574.x bank), accession number ON227496 for mitochondrion and Demes, K. W., Graham, M. H., & Suskiewicz, T. S. (2009). ON227495 for chloroplast. Phenotypic plasticity reconciles incongruous molecular and morphological taxonomies: The giant kelp, macrocystis (Laminariales, Phaeophyceae), is a monospecific genus. Author contribution Journal of Phycology, 45, 1266–1269. doi:10.1111/j.1529- 8817.2009.00752.x C. Iha: conceptualization, methodology, formal analysis, Dierckxsens, N., Mardulyn, P., & Smits, G. (2016). investigation, data curation, writing – original draft, writing – Novoplasty: de novo assembly of organelle genomes from review & editing, visualization. C. Layton: conceptualization, whole genome data. Nucleic Acids Research, 45, e18. doi:10. resources, writing – review & editing. W. Flentje: writing – 1093/nar/gkw955 review & editing, project administration, funding acquisition. Durrant, H. M. S., Barrett, N. S., Edgar, G. J., Coleman, M. A., A. Lenton: writing – review & editing, project administration, & Burridge, C. P. (2015). Shallow phylogeographic histories funding acquisition. C. Johnson: conceptualization, resources, of key species in a biodiversity hotspot. Phycologia, 54, writing – review & editing. C.I. Fraser: conceptualization, 556–565. doi:10.2216/15-24.1 writing – review & editing. A. Willis: conceptualization, writ- Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment ing – review & editing, project administration, funding acqui- with high accuracy and high throughput. Nucleic Acids sition, supervision. Research, 32, 1792–1797. doi:10.1093/nar/gkh340 Estes, J. A., & Steinberg, P. (1988). Predation, herbivory, and kelp evolution. Paleobiology, 14, 19–36. doi:10.1017/ References S0094837300011775 Graf, L., Kim, Y. J., Cho, G. Y., Miller, K. A., Yoon, H. S., & Andrews, S. 2010. FastQC: A quality control tool for high Li, X. -Q. (2017). Plastid and mitochondrial genomes of throughput sequence data. http://www.bioinformatics.bab Coccophora langsdorfii (Fucales, Phaeophyceae) and the raham.ac.uk/projects/fastqc/ . utility of molecular markers. PLoS One, 12, e0187104. Astorga, M. P., Hernández, C. E., Valenzuela, C. P., Avaria- doi:10.1371/journal.pone.0187104 Llautureo, J., & Westermeier, R. (2012). Origin, diversifica- Graham, M. H., Vasquez, J. A., & Buschmann, A. H. (2007). tion, and historical biogeography of the giant kelps genus Global ecology of the giant kelp Macrocystis: From ecotypes macrocystis: evidences from bayesian phylogenetic analysis. to ecosystems. Oceanography and Marine Biology, 45, Revista de Biología Marina Y Oceanografía, 47, 573–579. 39–88. doi:10.4067/S0718-19572012000300019 Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q., Boalch, G. T. 1981. Do we really need to grow macrocystis in & Vinh, L. S. (2018). Ufboot2: Improving the ultrafast Europe? In: T. Levring. [Ed.] Xth International Seaweed bootstrap approximation. Molecular Biology and Symposium: Proceedings Göteborg, Sweden August 11-15, Evolution, 35, 518–522. doi:10.1093/molbev/msx281 1980. Göteborg, Sweden, pp. 657–667. Iha, C., Grassa, C. J., Lyra, G. M., Davis, C. C., Verbruggen, H., Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: Oliveira, M. C., & Müller, K. (2018). Organellar genomics: A flexible trimmer for Illumina sequence data. A useful tool to study evolutionary relationships and mole- Bioinformatics, 30, 2114–2120. doi:10.1093/bioinfor cular evolution in Gracilariaceae (Rhodophyta). Journal of matics/btu170 Phycology, 54, 775–787. doi:10.1111/jpy.12765 Butler, C. L., Lucieer, V. L., Wotherspoon, S. J., & Johnson, C. R., Banks, S. C., Barrett, N. S., Cazassus, F., Johnson, C. R. (2020). Multi-decadal decline in cover of Dunstan, P. K., Edgar, G. J. . . . Taw, N. (2011). Climate giant kelp macrocystis pyrifera at the southern limit of its change cascades: Shifts in oceanography, species’ ranges Australian range. Marine Ecology Progress Series, 653, 1–18. and subtidal marine community dynamics in eastern doi:10.3354/meps13510 Tasmania. Journal of Experimental Marine Biology and Camus, C., Faugeron, S., & Buschmann, A. H. (2018). Ecology, 400, 17–32. doi:10.1016/j.jembe.2011.02.032 Assessment of genetic and phenotypic diversity of the giant kelp, Macrocystis pyrifera, to support breeding Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von programs. Algal Research, 30, 101–112. doi:10.1016/j.algal. Haeseler, A., & Jermiin, L. S. (2017). ModelFinder: Fast 2018.01.004 model selection for accurate phylogenetic estimates. Chen, J., Zang, Y., Shang, S., & Tang, X. (2019). The complete Nature Methods, 14, 587–589. doi:10.1038/nmeth.4285 mitochondrial genome of the brown alga macrocystis integ- Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read rifolia (Laminariales, Phaeophyceae). Mitochondrial DNA alignment with Bowtie 2. Nature Methods, 9, 357–359. Part B, 4, 635–636. doi:10.1080/23802359.2018.1495114 doi:10.1038/nmeth.1923 86 C. IHA ET AL. Layton, C., Coleman, M. A., Marzinelli, E. M., Steinberg, P. D., Oudot-Le Secq, M. P., Loiseaux-de Goer, S., Stam, W. T., Swearer, S. E., Vergés, A. . . . Johnson, C. R. (2020). Kelp & Olsen, J. L. (2006). Complete mitochondrial genomes forest restoration in Australia. Frontiers in Marine Science, of the three brown algae (Heterokonta: Phaeophyceae) 7, 74. doi:10.3389/fmars.2020.00074 dictyota dichotoma, fucus vesiculosus and desmarestia Layton, C., & Johnson, C. R. 2021. Assessing the feasibility of viridis. Current Genetics, 49, 47–58. doi:10.1007/ restoring giant kelp forests in Tasmania. Report to the s00294-005-0031-4 National Environmental Science Program, Marine Peters, J. C., Waters, J. M., Dutoit, L., & Fraser, C. I. (2020). Biodiversity Hub. SNP analyses reveal a diverse pool of potential colonists to Leigh, J. W., Bryant, D., Nakagawa, S., & Nakagawa, S. (2015). earthquake-uplifted coastlines. Molecular Ecology, 29, Popart full-feature software for haplotype network 149–159. doi:10.1111/mec.15303 construction. Methods in Ecology and Evolution, 6, Prjibelski, A., Antipov, D., Meleshko, D., Lapidus, A., & 1110–1116. doi:10.1111/2041-210X.12410 Korobeynikov, A. (2020). Using SPAdes De Novo Löytynoja, A. (2014). Phylogeny-aware alignment with Assembler. Current Protocols in Bioinformatics, 70, e102. PRANK. In D. J (Ed.), In: Russell (pp. 155–170). Totowa, doi:10.1002/cpbi.102 NJ: Humana Press. Schiel, D. R., & Foster, M. S. (2015). The biology and ecology of Lyra, G. M., Iha, C., Grassa, C. J., Cai, L., Zhang, H., giant kelp forests (p. 416). University of California Press. Lane, C. . . . Davis, C. C. (2021). Phylogenomics, diver- Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., gence time estimation and trait evolution provide a new Hartmann, M., Hollister, E. B. . . . Weber, C. F. (2009). look into the Gracilariales (Rhodophyta). Molecular Introducing mothur: open-source, platform-independent, Phylogenetics and Evolution, 165, 107294. doi:10.1016/j. community-supported software for describing and compar- ympev.2021.107294 ing microbial communities. Applied and Environmental Macaya, E. C., & Zuccarello, G. C. (2010a). DNA barcoding Microbiology, 75, 7537–7541. doi:10.1128/AEM.01541-09 and genetic divergence in the giant kelp macrocystis Shen, W., Le, S., Li, Y., Hu, F., & Zou, Q. (2016). SeqKit: A (Laminariales). Journal of Phycology, 46, 736–742. doi:10. cross-platform and ultrafast toolkit for FASTA/Q file 1111/j.1529-8817.2010.00845.x manipulation. PLoS One, 11, e0163962. doi:10.1371/jour Macaya, E. C., & Zuccarello, G. C. (2010b). Genetic structure nal.pone.0163962 of the giant kelp Macrocystis pyrifera along the southeastern Starko, S., Bringloe, T. T., Gomez, M. S., Darby, H., Pacific. Marine Ecology Progress Series, 420, 103–112. Graham, S. W., Martone, P. T., & Piganeau, G. (2021). doi:10.3354/meps08893 Genomic rearrangements and sequence evolution across Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., brown algal organelles. Genome Biology and Evolution, 13, Woodhams, M. D., von Haeseler, A., & Lanfear, R. (2020). evab124. doi:10.1093/gbe/evab124 IQ-TREE 2: New models and efficient methods for phylo- Starko, S., Soto Gomez, M., Darby, H., Demes, K. W., genetic inference in the genomic era. Molecular Biology and Kawai, H., Yotsukura, N. . . . Martone, P. T. (2019). Evolution, 37, 1530–1534. doi:10.1093/molbev/msaa015 A comprehensive kelp phylogeny sheds light on the evolu- Mora‐soto, A., Capsey, A., Friedlander, A. M., Palacios, M., tion of an ecosystem. Molecular Phylogenetics and Brewin, P. E., Golding, N. . . . Palmeirim, A. F. (2021). One Evolution, 136, 138–150. doi:10.1016/j.ympev.2019.04.012 of the least disturbed marine coastal ecosystems on Earth: Szymanski, M., Zielezinski, A., Barciszewski, J., Spatial and temporal persistence of Darwin’s sub‐Antarctic Erdmann, V. A., & Karlowski, W. M. (2016). 5srnadb: An giant kelp forests. Journal of Biogeography, 48, 2562–2577. information resource for 5S ribosomal RNAs. Nucleic Acids doi:10.1111/jbi.14221 Research, 44, D180–3. doi:10.1093/nar/gkv1081 Oudot-Le Secq, M. P., Fontaine, J. M., Rousvoal, S., Wickham, H. (2016). Ggplot2: Elegant graphics for data ana- Kloareg, B., & Loiseaux-De Goer, S. (2001). The complete lysis (p. 276). Springer-Verlag New York. sequence of a brown algal mitochondrial genome, the ecto- Yang, Z. (2007). PAML 4: Phylogenetic analysis by maximum carpale pylaiella littoralis (L.) Kjellm. Journal of Molecular likelihood. Molecular Biology and Evolution, 24, 1586–1591. Evolution, 53, 80–88. doi:10.1007/s002390010196 doi:10.1093/molbev/msm088
http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png
Applied Phycology
Taylor & Francis
http://www.deepdyve.com/lp/taylor-francis/organellar-genomes-of-giant-kelp-from-the-southern-hemisphere-AU7yVdtdg8
