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Genomics Reveals Abundant Speciation in the Coral Reef Building Alga Porolithon Onkodes (Corallinales, Rhodophyta)1

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Genomics Reveals Abundant Speciation in the Coral Reef Building Alga Porolithon Onkodes (Corallinales, Rhodophyta)1 J. Phycol. 54, 429–434 (2018) © 2018 Phycological Society of America DOI: 10.1111/jpy.12761 L ETTER GENOMICS REVEALS ABUNDANT SPECIATION IN THE CORAL REEF BUILDING ALGA POROLITHON ONKODES (CORALLINALES, RHODOPHYTA)1 Paul W. Gabrielson , Jeffery R. Hughey and Guillermo Diaz-Pulido An essential suite of coral reef ecosystem engineers is coralline red algae. Among these, the smooth, encrusting Porolithon onkodes has historically been considered the most important and common reef building species worldwide. We assess P. onkodes biodiversity by performing a genomic analysis of the lectotype specimen collected in 1892 from the Tami Islands, Gulf of Huon, east of New Guinea. Comparisons of DNA sequences from the lectotype specimen to those deposited in GenBank and to newly generated sequences from both field-collected and historical specimens demonstrate that at least 20 distinct species are passing under P. onkodes. We hypothesize that there were multiple evolutionary drivers including ecophysiology, hydrodynamic regimes, and biotic interactions as well as historical biogeography, which resulted in this high diversity of smooth, encrusting Porolithon species throughout the tropics. Our results emphasize the need to document the biodiversity, ecophysiology, and habitats of these tropical, reef-building algae in light of climate change and ocean acidification. Porolithon onkodes is currently 2014). Both of these Porolithon his new genus, Porolithon (Foslie recognized worldwide as the species are distinguished by their 1909). Following earlier successes major coral reef cementing and smooth, encrusting habitat in con- characterizing organellar genomes armoring coralline red alga, pro- trast to other fore reef corallines of red algal type specimens viding structural integrity to fore that form densely branched more (Hughey et al. 2014, 2017, Boo reef habitats (Maneveldt and or less hemispherical mounds. et al. 2016), we analyzed the lec- Keats 2014). The importance of Beginning in the late 1960s and totype of L. onkodes and compared nongeniculate coralline red algae continuing to the present, the its DNA to recent field-collected to coral reef formation was first ecological niches thought to be specimens. The lectotype DNA recognized by Charles Darwin occupied by P. onkodes have was extracted from a 2 9 2mm2 (1890), “Nothing can be more sin- expanded to include back reef fragment following Hernandez- gular than the appearance at low rubble-filled moats as well as slope Kantun et al. (2016) and imple- tide of this ‘flat’ of naked stone, habitats to 5–10 m depth menting the guidelines proposed especially where it is externally (Womersley and Bailey 1970, Lee by Hughey and Gabrielson bounded the smooth convex 1978, Adey et al. 1982). (2012). Illumina 76 bp paired-end mound of Nulliporae appearing Seven coralline species were library and sequencing was car- like a breakwater built to resist described based on specimens ried out by myGenomics LLC using the waves.” Ever since, throughout from the Tami Islands, Gulf of an in-house low-input protocol the tropical Pacific and Indian Huon, collected by native divers (http://www.mygenomics.com). Oceans, P. onkodes has been cited in 1–3 m of water in March 1892 For all other samples, the DNA as the most important species pro- and communicated by the was extracted, amplified, and San- viding major cover on windward Lutheran missionary Rev. Georg ger sequenced following Gabriel- fore reefs from the intertidal reef Bamler, including the coral tine son et al. (2011) and Adey et al. ridge and continuing seaward encrusting Lithothamnion onkodes (2015). Genomic data were assem- through the reef crest and rim (Heydrich 1897), basionym of bled with the default de novo set- (Howe 1912, Setchell 1926, Taylor P. onkodes (Fig. S1 in the Support- tings in CLC Genomics â 1950, Doty and Morrison 1954, ing Information). Much of this Workbench 9.5.2 ( 2016 CLC bio, Marsh 1970, Littler and Doty collection was destroyed in the a QIAGEN Company, German- 1975, Dean et al. 2015). Its eco- bombing of the Berlin Museum town, MD, USA), Velvet 1.2.08 logical counterpart in the Carib- during World War II, but before with a kmer of 59 (Zerbino and bean Sea was known as Porolithon 1909, Heydrich sent a specimen Birney 2008), and default settings pachydermum (Adey 1967), until of L. onkodes to his coralline com- in IDBA-UD (Peng et al. 2012). placed into synonymy under petitor, Mikhail Foslie, in Trond- The three assemblers indepen- P. onkodes (Maneveldt and Keats heim, Norway, who placed it in dently yielded the same results. 429 430 PAUL W. GABRIELSON ET AL. Genome gaps were closed by PCR and contains 228 genes dermum are the same species, with and sequencing and by iterative (Table S2). It has a high level of P. antillarum having nomenclatu- mapping with Geneious 8.1.5 gene synteny with the two previ- ral priority. Just as there are multi- (BioMatters, Auckland, New Zeal- ously published genomes of Cal- ple species passing under and). Genomes were annotated liarthron tuberculosum and P. onkodes in the Indo-Pacific, using NCBI ORFfinder and align- Sporolithon durum (Janouskovec there are at least two other species ments obtained via BLASTX et al. 2013, Lee et al. 2016). The passing under P. antillarum in the against the reference sequences of mitogenome of Porolithon onkodes tropical western Atlantic (Fig. 1, Calliarthron tuberculosum (GenBank is 27,882 bp and contains 46 represented by MF979946 and accessions KC153978 and genes (Table S3). The mitogen- MF979960). There are four KR005619). tRNAs were identified ome is similar in gene content to unnamed specimens in GenBank using tRNAscan-SE 1.21 web ser- other corallines (C. tuberculosum, (LCB0701, LCB9658, LCB0712, ver (Schattner et al. 2005) and Corallina officinalis, and S. durum); LCB0678), all from Fiji and all rRNAs using RNAmmer 1.2 (Lage- however, it differs in organization with vague habitat data (“isolated ETTER sen et al. 2007). Locally Collinear (Fig. S2 in the Supporting Infor- by scuba diving or on the shore at L Block (LCB) alignments were gen- mation). Most noteworthy, riboso- low tide”), whose psbA erated using ProgressiveMauve mal proteins rps12 and rpl20, the (GQ917931, GQ917955, GQ917 with a seed of 21 with the “Use small subunit rRNA, and nad4L of 964, GQ917969) and mitochon- seed families” option selected the NR segment (Yang et al. drial-encoded COI (GQ917588, (Darling et al. 2010). Sequences 2015) are situated with the CY GQ917571, GQ917592, GQ917 of the plastid genome (GenBank segment, and the tRNAs (R, Y, V, 276) gene sequences indicate that KY212106), mitogenome (Gen- N) are flanking orf172 following they are P. onkodes (for psbA <0.4% Bank KY212107), and nuclear the large subunit rRNA. diverged, Hind et al. 2016, for ribosomal cistron (GenBank Maximum Likelihood (ML) COI <4.5% diverged, Saunders KY212108) were deposited in Gen- phylogenetic analyses of the plas- 2005). None of the other Bank. DNA sequences of the rbcL tid-encoded rbcL gene (Fig. 1) and P. onkodes GenBank sequences of gene and multiple genes (SSU, multigene trees (Fig. S3 in the any marker, including those listed LSU, psbA, COX1, 23S, rbcL) rep- Supporting Information), based as Hydrolithon onkodes, are resenting published and unpub- on newly generated sequences or P. onkodes, but all belong in Poroli- lished Porolithon, and unidentified sequences from GenBank thon except KM369154 from New coralline algae were downloaded (Table S3), showed that over 20 Zealand (Fig. 1). The distributions from GenBank (Table S1 in the species are passing under the of the Porolithon species for which Supporting Information) and name Porolithon onkodes. rbcL we have rbcL sequences are shown aligned with MAFFT (Katoh and sequences from the 30 end of the in Figure 2. Species level status is Standley 2013). Maximum likeli- gene (rbcL-3P) were also obtained based on rbcL pair-wise sequence hood analyses were executed with from the type specimens of divergences >1% (Table S4 in the T-REX (Boc et al. 2012) and the P. sandvicense (basionym: Lithophyl- Supporting Information), a con- GTR + gamma model with 1,000 lum dentatum f. sandvicensis, type servative value given that 0.5%– fast bootstraps. The Bayesian anal- locality Sandwich Islands, now 0.8% has been used to distinguish ysis (Ronquist and Huelsenbeck Hawaiian Islands), P. oligocarpum coralline species in other genera 2003) was performed using the (basionym: Lithophyllum oligo- of Corallinales (Gabrielson et al. same model with default settings carpum, type locality: Puerto Oro- 2011, Hind et al. 2016). in Geneious. The rbcL tree was tava [Puerto de la Cruz], Tenerife, It is clear from the DNA rooted with Harveylithon sp. (Gen- Canary Islands), P. pachydermum sequence data based on multiple Bank MF979962) and the multi- (basionym: Lithophyllum onkodes f. genetic markers that the evolution gene tree with Harveylithon rupestre pachydermum, type locality: Vestin- of tropical and subtropical (SSU, GenBank KM073303; psbA, dien = Danish West Indies, now smooth, encrusting Porolithon spe- KM407535). Phylogenetic trees U.S. Virgin Islands), and P. antil- cies is not marked by morpho-ana- were visualized with TreeDyn larum (basionym: Lithophyllum tomical discontinuities and that 198.3 at Phylogeny.fr (Dereeper antillarum type locality: Culebra none of the morpho-anatomical et al. 2008). Island, Puerto Rico). All of these studies of the past 100+ years has Analysis of the lectotype of species were recently proposed as enabled us to recognize the Lithothamnion onkodes resulted in synonyms of P. onkodes based on numerous species passing under the complete plastid (Table S2 in morpho-anatomical characters P. onkodes. Sequenced specimens, the Supporting Information) and (Maneveldt and Keats 2014, Gal- for which we also have good habi- mitochondrial (Table S3 in the lardo et al. 2016). Not one of tat data, indicate that species evo- Supporting Information) genomes them is P. onkodes (Fig. 1). Poroli- lution has been complex with as well as the ribosomal cistron.
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