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Taxonomic Notes on Caribbean Neosiphonia and Polysiphonia (Ceramiales, Florideophyceae): Five Species from Florida, USA and Mexico

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Taxonomic Notes on Caribbean Neosiphonia and Polysiphonia (Ceramiales, Florideophyceae): Five Species from Florida, USA and Mexico Article in press - uncorrected proof Botanica Marina 54 (2011): 269–292 ᮊ 2011 by Walter de Gruyter • Berlin • Boston. DOI 10.1515/BOT.2011.036 Taxonomic notes on Caribbean Neosiphonia and Polysiphonia (Ceramiales, Florideophyceae): five species from Florida, USA and Mexico Nadya R. Mamoozadeh and D. Wilson Freshwater* evidence’’ to determine which morphological characters are Center for Marine Science, UNCW, 5600 Marvin Moss relevant to species identification. The recent coupling of Lane, Wilmington, NC 28409, USA, morphological characters with DNA sequence data is helping e-mail: [email protected] establish an accurate classification of Polysiphonia based on natural relationships. * Corresponding author Molecular-assisted identification (MAI) through use of the plastid-encoded ribulose-1,5-bisphosphate carboxylase/oxy- genase large subunit gene (rbcL) has proven useful for dis- Abstract criminating species of Polysiphonia s.l. Previous studies of rbcL sequence data in Polysiphonia s.l. detected compara- Molecular-assisted identification using plastid-encoded rbcL tively low intraspecific and high interspecific sequence and mitochondrion-encoded COI loci identified five species divergences, with values ranging from 0 to 1.3% (with an of Polysiphonia sensu lato from 16 Florida and Caribbean Mexico samples. Morphological character states were exam- instance of 2.13%) and 2.6–14.12%, respectively (McIvor et ined and used to identify these species as Neosiphonia baja- al. 2001, Kim et al. 2004, Kim and Yang 2005). A relatively cali comb. nov., N. echinata comb. nov., N. sphaerocarpa, distinct break between intra- and interspecific sequence var- N. tepida, and Polysiphonia anomala. Descriptions are pro- iation makes rbcL a useful tool for aiding species identi- vided and the phylogenetic relationships of the five species fications. were determined through maximum likelihood analyses of The 59 end of the mitochondrion-encoded cytochrome c rbcL and nuclear-encoded SSU sequence data. Neosiphonia oxidase subunit I gene (COI) is another region of DNA that bajacali and N. echinata had a combination of character is employed for MAI. Previous studies of red algae have states described for Neosiphonia: rhizoids cut-off from peri- shown COI to be successful in distinguishing closely related central cells, lateral branch or trichoblast initials on every and cryptic species as well as geographic groups within a segment in a spiral pattern, tetrasporangia in spiral series, species (Saunders 2005, Robba et al. 2006, Yang et al. 2008, and spermatangial stichidia developing as bifurcations of Clarkston and Saunders 2010, Le Gall and Saunders 2010). trichoblasts, and these new combinations are proposed. The utility of COI barcoding within Polysiphonia s.l. has yet Examination of N. echinata, P. fracta and North Carolina to be established. specimens identified as P. breviarticulata revealed no signif- Phylogenetic relationships among Polysiphonia s.l. species icant morphological differences. Polysiphonia fracta is pro- can also be determined using molecular data. The nuclear- posed as a synonym of N. echinata and the presence of P. encoded 18S rDNA (SSU) gene has limited intraspecific breviarticulata within the western Atlantic is questioned. sequence variation and provides better resolution of taxo- This is the first report of N. bajacali from the Caribbean and nomic relationships above the species level. Analyses of SSU the first report of N. echinata from Caribbean Mexico. sequence data showed that Polysiphonia s.l. is polyphyletic with respect to other genera (Choi et al. 2001). The rbcL Keywords: Caribbean Mexico; Florida; molecular-assisted locus has a faster rate of evolution than SSU allowing greater identification; Neosiphonia; Polysiphonia. resolution of species-level relationships. The use of rbcLto determine species relationships has been common in recent studies of Polysiphonia s.l. (McIvor et al. 2001, Kim et al. Introduction 2004, 2005, Stuercke and Freshwater 2008, 2010). Phylo- genetic relationships within Polysiphonia s.l. can be thor- Polysiphonia Greville (Rhodomelaceae) is a large (ca. 200 oughly evaluated when analyses of SSU and rbcLare species) red algal genus whose species have a nearly global compared with one another (Stuercke 2006). distribution. Species of Polysiphonia sensu lato (s.l.) have a Stuercke and Freshwater (2008) examined many of the delicate habit composed of filamentous main axes and morphological characters used to distinguish Polysiphonia branches that are segmented and polysiphonous. A wide s.l. species in an integrated molecular-morphological study. range of morphological variability occurs among the many Little to no intraspecific variation was found in the character species of Polysiphonia s.l. This variation has led to much states for pericentral cell number, rhizoid-pericentral cell debate on the classification of species within the genus. To connection, lateral branch-trichoblast relationship, sperma- revise the classification of Polysiphonia s.l., Kim et al. tangial axis development, tetrasporangial arrangement, tri- (2000) suggested the use of ‘‘independent comparative choblasts/scar cell occurrence and pattern, holdfast type, and Brought to you by | College of William and Mary 2010/101 Authenticated | 128.239.99.140 Download Date | 1/13/14 7:32 PM Article in press - uncorrected proof 270 N.R. Mamoozadeh and D.W. Freshwater: Five Neosiphonia/Polysiphonia species from the Caribbean cicatrigenous branch formation. The genus Neosiphonia follow the Index Herbariorum (http://sciweb.nybg.org/sci- M.-S. Kim et I.K. Lee was segregated from Polysiphonia ence2/IndexHerbariorum.asp). based on a combination of character states including the fol- lowing from those listed above: rhizoids that are cut-off from Morphological data pericentral cells, spirally arranged trichoblasts or scar cells on every segment, three-celled carpogonial branches, sper- Specimens and slides were observed using an Olympus SZH matangial axes developing as a bifurcation of trichoblasts, dissecting microscope (Olympus America Inc., Center and spirally arranged tetrasporangia (Kim and Lee 1999). Valley, PA, USA) and a Nikon Labophot-2 compound micro- Polysiphonia s.l. now includes species that are predomi- scope (Nikon Inc., Melville, NY, USA). Images were cap- nantly placed in Neosiphonia or Polysiphonia, although less tured using a Zeiss Axio Imager.Z1 compound microscope speciose genera are also included. fitted with an AxioCam MRc 5 camera system (Carl Zeiss Study of the Caribbean marine algal flora has resulted in Microimaging Inc., Thornwood, NY, USA) or an Olympus reports of at least 28 distinct species of Polysiphonia s.l. BX41 compound microscope fitted with a Roper Scientific (e.g., Wynne 1998). Early reports of Polysiphonia s.l. by Photometrics᭨ CoolSnapTM camera (Photometrics, Tucson, Harvey (1853) and Børgesen (1918), described several spe- AZ, USA). Species descriptions were written based on obser- cies from Florida, USA and the West Indies, respectively. vations of specimens collected in this study and at the US, More recent reports are the result of floristic assessments and with information from the literature included for char- made throughout the Caribbean (e.g., Taylor 1929, 1941, acter states that were not directly observed. 1942, 1945, 1960, 1969, Almodovar and Ballantine 1983, Ballantine and Aponte 1997, Littler and Littler 2000, Mateo- DNA extraction and sequencing Cid et al. 2006). Caribbean studies specific to Polysiphonia s.l. include reports of species from Belize (Kapraun and Nor- DNA was extracted from specimens according to Hughey et ris 1982), Colombia and Venezuela (Kapraun et al. 1983). al. (2001) with an additional cleaning step using the One- The purpose of this study was to complete integrated Step௣ PCR Inhibitor Removal Kit (Zymo Research, Orange, molecular and morphological analyses of Polysiphonia s.l. CA, USA). SSU, rbcL, and COI were amplified following samples collected from Caribbean Mexico and Florida. the basic PCR recipe outlined in Freshwater et al. (2005) but Examination of morphology and MAI using rbcL and COI using GOTaq DNA polymerase and buffer (Promega, Mad- sequence data were used to identify four Neosiphonia and ison, WI, USA). The thermocycling protocol followed Fresh- one Polysiphonia species within samples while phylogenetic water et al. (2000) but with 35 cycles of denaturing, analyses of rbcL and SSU sequence data were used to deter- annealing at 40, 45, or 508C, and an elongation period of mine the relationships of these species. 90 s. Amplification products were cleaned with a Stratagene StrataPrep᭨ PCR Purification Kit (Stratagene, La Jolla, CA, USA) and used as templates in BigDye᭨ Terminator v3.1 sequencing reactions (Applied Biosystems, Foster City, CA, Materials and methods USA). Sequences were edited and assembled using Sequen- cher௣ (version 4.9, GeneCodes Corporation, Ann Arbor, MI, Collections and vouchers USA). Primers utilized in amplification and sequencing reac- tions are listed in Table 1. Samples of Neosiphonia and Polysiphonia were collected rbcL and COI sequences were generated for as many sam- from intertidal and subtidal substrata in Caribbean Mexico ples as possible. These loci are appropriate for the exami- and Florida by snorkeling (Appendix 1). Samples were dried nation of inter- and intraspecific relationships and were used in silica gel desiccant (Chase and Hills 1991) and deposited as barcodes to objectively assign samples to species (e.g.,
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