Splitting blades: why genera need to be more carefully defined; the case for Pyropia (Bangiales, Rhodophyta)

Zuccarello, Giuseppe C.,Wen, Xinging,Kim, Gwang Hoon The Korean Society of Phycology 2022 ALGAE Vol.37 No.3

The trend in naming genera based almost exclusively on molecular data, and not on morphological diagnostic characters, is increasing. In bifurcating phylogenetic trees generic cut-offs are arbitrary, but at the bare minimum nomenclatural changes should be supported by multiple phylogenetic methodologies using appropriate models for all the various gene partitions, strong support with all branch support methods, and should also result in adding to our knowledge of the interrelationships of taxa. We believe that a recent taxonomic treatment of the genus Pyropia (Yang et al. 2020) into several genera is unwarranted. We reanalysed the data presented in the recent article, using additional phylogenetic methods. Our results show that many of the newly established genera are not well supported by all methods, and the new circumscription of the genus Pyropia renders it unsupported. We also tested additional outgroups, which were previously suggested as sister to Pyropia, but this did not substantially change our conclusions. These generic nomenclatural changes of the previously strongly supported genus Pyropia, do not shed light on the evolution of this group and have serious consequences in these commercially important algae, that are also governed by a plethora of regulation and by-laws that now need to be amended. We suggest that the over-splitting of groups based only on poorly produced and modestly supported phylogenies should not be accepted and that the genus Pyropia sensu Sutherland et al. (2011) be restored.

Insights into evolution and speciation in the red alga Bostrychia: 15 years of research

Zuccarello, Giuseppe C.,West, John A. The Korean Society of Phycology 2011 ALGAE Vol.26 No.1

Studies of the red algal genus Bostrychia over the last 15 years have made it a model system for many evolutionary processes within red algal species. The combination of newly developed, or first employed methods, in red algal species studies has made Bostrychia a pioneer genus in intraspecific studies. Bostrychia was the first genus in which a mitochondrial marker was used for intraspecific red algal phylogeny, and the first for which a 3-genome phylogeny was undertaken. The genus was the first red alga used to genetically show maternal plastid and mitochondria inheritance, and also to show correlation between cryptic species (genetically divergent intraspecific lineages) and reproductive incompatibility. The chemotaxonomic use, and physiological function of osmolytes, has also been extensively studied in Bostrychia. Our continuous studies of Bostrychia also highlight important aspects in algal species studies. Our worldwide sampling, and resampling in certain areas, show that intensive sampling is needed to accurately assess the genetic diversity and therefore phylogeographic history of algal species, with increased sampling altering evolutionary hypotheses. Our studies have also shown that long-term morphological character stability (stasis) and character convergence can only be correctly assessed with wide geographic sampling of morphological species. While reproductive incompatibility of divergent lineages supports the biological species nature of these lineages, reproductive incompatibility is also seen between isolates with little genetic divergence. It seems that reproductive incompatibility may evolve quickly in red algae and the unique early stages of fertilization (e.g., gametes covered by walls, active movement of spermatium nuclei to the distant egg nucleus), also well investigated in Bostrychia,. may be key to our understanding of this process.

Phylogeography of the Lessonia variegata species complex (Phaeophyceae, Laminariales) in New Zealand

Zuccarello, Giuseppe C.,Martin, Peter The Korean Society of Phycology 2016 ALGAE Vol.31 No.2

A goal of phylogeography is to relate phylogenetic patterns to potential historic and contemporary geographic isolating events. Genetic breaks found in phylogeographic studies may denote boundaries between more generally applicable biogeographic regions. We investigated the distribution of Lessonia variegata, an important habitat forming alga, found on most rocky shores around New Zealand’s main islands, plus related species from surrounding waters. L. variegata has been shown to consist of four distinct cryptic species. Our aim was to compare the distribution of L. variegata with proposed bioregions; and to develop phylogeographic hypotheses to explain its present day distribution. Both a mitochondrial (atp8-sp) and plastid (RuBisCo spacer) marker, with different mutation rates, were used to gain information of the phylogenetic history of Lessonia. The data revealed high phylogeographic structuring and reciprocal endemism for all L. variegata cryptic species. One species (L. variegata / N) is confined to the northern part of the North Island of New Zealand; L. variegata / W is found at the southeast of the North Island and the northern South Island; L. variegata / K is endemic to the northeast South Island; and L. variegata / S is restricted to the southern part of the South Island. No overlapping areas of L. variegata species distribution were found. The data showed that genetic breaks in Lessonia do mostly correlate to bioregions, and highlight the importance of Cape Campbell at the northeast of the South Island and East Cape in the North Island, well known phylogeographic breaks, as a barrier between adjacent species.

ERRATUM: Author's Name Correction

Giuseppe C., Zuccarello,Xinging, Wen,Gwang Hoon, Kim The Korean Society of Phycology 2022 ALGAE Vol.37 No.4

Insights into evolution and speciation in the red alga Bostrychia: 15 years of research

Giuseppe C. Zuccarello,John A. West 한국조류학회I 2011 ALGAE Vol.26 No.1

Studies of the red algal genus Bostrychia over the last 15 years have made it a model system for many evolutionary processes within red algal species. The combination of newly developed, or first employed methods, in red algal species studies has made Bostrychia a pioneer genus in intraspecific studies. Bostrychia was the first genus in which a mitochondrial marker was used for intraspecific red algal phylogeny, and the first for which a 3-genome phylogeny was undertaken. The genus was the first red alga used to genetically show maternal plastid and mitochondria inheritance, and also to show correlation between cryptic species (genetically divergent intraspecific lineages) and reproductive incompatibility. The chemotaxonomic use, and physiological function of osmolytes, has also been extensively studied in Bostrychia. Our continuous studies of Bostrychia also highlight important aspects in algal species studies. Our worldwide sampling, and resampling in certain areas, show that intensive sampling is needed to accurately assess the genetic diversity and therefore phylogeographic history of algal species, with increased sampling altering evolutionary hypotheses. Our studies have also shown that long-term morphological character stability (stasis) and character convergence can only be correctly assessed with wide geographic sampling of morphological species. While reproductive incompatibility of divergent lineages supports the biological species nature of these lineages, reproductive incompatibility is also seen between isolates with little genetic divergence. It seems that reproductive incompatibility may evolve quickly in red algae and the unique early stages of fertilization (e.g., gametes covered by walls, active movement of spermatium nuclei to the distant egg nucleus), also well investigated in Bostrychia, may be key to our understanding of this process.

Holocarpic oomycete parasites of red algae are not Olpidiopsis, but neither are they all Pontisma or Sirolpidium (Oomycota)

Giuseppe C. Zuccarello,Claire M. M. Gachon,Yacine Badis,Pedro Murúa,Andrea Garvetto,Gwang Hoon Kim 한국조류학회I 2024 ALGAE Vol.39 No.1

Oomycetes are ubiquitous heterotrophs of considerable economic and ecological importance. Lately their diversity in marine environments has been shown to be greatly underappreciated and many lineages of intracellular holocarpic parasites, infecting micro- and macro-algae, remain to be fully described taxonomically. Among them, pathogens of marine red algae have been studied extensively as they infect important seaweed crops. Throughout the 20th century, most intracellular, holocarpic biotrophic oomycetes that infect red algae have been assigned to the genus Olpidiopsis Cornu. However, 18S rRNA sequencing of Olpidiopsis saprolegniae, the species considered the generitype for Olpidiopsis, suggests that this genus is not closely related to the marine pathogens and that the latter requires a nomenclatural update. Here, we compile and reanalyze all recently published 18S rRNA sequence data for marine holocarpic oomycetes, with a particular focus on holocarpic pathogens of red algae. Their taxonomy has been revised twice over the past four years, with suggestions to transfer them first into the genus Pontisma and then Sirolpidium, and into a monogeneric order, Pontismatales. We show however, that previously published topologies and the proposed taxa Pontisma, Sirolpidium, and Pontismatales are unsupported. We highlight that name changes that are unfounded and premature create confusion in interested parties, especially concerning pathogens of marine red algae that infect important seaweed crops. We thus propose that the names of these holocarpic biotrophic parasites of red algae are retained temporarily, until a supported topology is produced with more genetic markers to enable the circumscription of species and higher-level taxa.

Phylogeography of the Lessonia variegata species complex (Phaeophyceae, Laminariales) in New Zealand

Giuseppe C. Zuccarello,Peter Martin 한국조류학회I 2016 ALGAE Vol.31 No.2

A goal of phylogeography is to relate phylogenetic patterns to potential historic and contemporary geographic isolating events. Genetic breaks found in phylogeographic studies may denote boundaries between more generally applicable biogeographic regions. We investigated the distribution of Lessonia variegata, an important habitat forming alga, found on most rocky shores around New Zealand’s main islands, plus related species from surrounding waters. L. variegata has been shown to consist of four distinct cryptic species. Our aim was to compare the distribution of L. variegata with proposed bioregions; and to develop phylogeographic hypotheses to explain its present day distribution. Both a mitochondrial (atp8-sp) and plastid (RuBisCo spacer) marker, with different mutation rates, were used to gain information of the phylogenetic history of Lessonia. The data revealed high phylogeographic structuring and reciprocal endemism for all L. variegata cryptic species. One species (L. variegata / N) is confined to the northern part of the North Island of New Zealand; L. variegata / W is found at the southeast of the North Island and the northern South Island; L. variegata / K is endemic to the northeast South Island; and L. variegata / S is restricted to the southern part of the South Island. No overlapping areas of L. variegata species distribution were found. The data showed that genetic breaks in Lessonia do mostly correlate to bioregions, and highlight the importance of Cape Campbell at the northeast of the South Island and East Cape in the North Island, well known phylogeographic breaks, as a barrier between adjacent species.

Biology of Porphyra pulchella sp. nov. from Australia and New Zealand

Ackland, Jillian C.,West, John A.,Scott, Joseph,Zuccarello, Giuseppe C.,Broom, Judy The Korean Society of Phycology 2006 ALGAE Vol.21 No.2

Porphyra pulchella sp. nov. Ackland, West, Scott and Zuccarello was obtained at Mimosa Rock National Park, New South Wales; Westgate Bridge, Victoria, Australia; and Waihau Bay, North Island, New Zealand. It occurs mainly in mangrove habitats and is very small (± 1 mm) in field collections. In laboratory culture at 21 ± 2°C tiny blades (0.5-3.0 mm) reproduced exclusively by archeospores liberated from vegetative cells of the upper sector of the blades. The archeospores displayed amoeboid and gliding motility once discharged. At 14 ± 2°C the blades grew to 25 mm and produced longitudinal spermatangial streaks mixed with ‘phyllosporangial’ streaks. The discharged ‘phyllospores’ showed amoeboid motility and germinated forming asexual blades. A conchocelis phase with typical bangiophycidean pit connections was observed in blade cultures after 8-10 weeks at 14 ± 2°C. Conchocelis filaments produced conchosporangia and these released amoeboid conchospores that developed into archeosporangiate blades. Molecular data indicate that all 3 isolates are genetically identical.

Biology of Porphyra pulchella sp. nov. fromAustralia and New Zealand

Jillian C. Ackland,John A. West,Joseph Scott,Giuseppe C. Zuccarello,Judy Broom 한국조류학회I 2006 ALGAE Vol.21 No.2

Porphyra pulchella sp. nov. Ackland, West, Scott and Zuccarello was obtained at Mimosa Rock National Park, New South Wales; Westgate Bridge, Victoria, Australia; and Waihau Bay, North Island, New Zealand. It occurs mainly in mangrove habitats and is very small (± 1 mm) in field collections. In laboratory culture at 21 ± 2°C tiny blades (0.5- 3.0 mm) reproduced exclusively by archeospores liberated from vegetative cells of the upper sector of the blades. The archeospores displayed amoeboid and gliding motility once discharged. At 14 ± 2°C the blades grew to 25 mm and produced longitudinal spermatangial streaks mixed with ‘phyllosporangial’ streaks. The discharged ‘phyllospores’ showed amoeboid motility and germinated forming asexual blades. A conchocelis phase with typical bangiophycidean pit connections was observed in blade cultures after 8-10 weeks at 14 ± 2°C. Conchocelis filaments produced conchosporangia and these released amoeboid conchospores that developed into archeosporangiate blades. Molecular data indicate that all 3 isolates are genetically identical.

Physiological responses to salt stress by native and introduced red algae in New Zealand

Gambichler, Vanessa,Zuccarello, Giuseppe C.,Karsten, Ulf The Korean Society of Phycology 2021 ALGAE Vol.36 No.2

Intertidal macroalgae are regularly exposed to hypo- or hypersaline conditions which are stressful. However, red algae in New Zealand are generally poorly studied in terms of salinity tolerance. Consequently, two native (Bostrychia arbuscula W. H. Harvey [Ceramiales], Champia novae-zelandiae [J. D. Hooker & Harvey] Harvey [Rhodymeniales]) and one introduced red algal taxon (Schizymenia spp. J. Agardh [Nemastomatales]) were exposed for 5 days in a controlled salt stress experiment to investigate photosynthetic activity and osmotic acclimation. The photosynthetic activity of B. arbuscula was not affected by salinity, as reflected in an almost unchanged maximum quantum yield (F_v/F_m). In contrast, the F_v/F_m of C. novae-zelandiae and Schizymenia spp. strongly decreased under hypo- and hypersaline conditions. Treatment with different salinities led to an increase of the total organic osmolyte concentrations with rising salt stress in B. arbuscula and Schizymenia spp. In C. novae-zelandiae the highest organic osmolyte concentrations were recorded at S_A 38, followed by declining amounts with further hypersaline exposure. In B. arbuscula, sorbitol was the main organic osmolyte, while the other taxa contained floridoside. The data presented indicate that all three red algal species conspicuously differ in their salt tolerance. The upper intertidal B. arbuscula exhibited a wide salinity tolerance as reflected by unaffected photosynthetic parameters and strong sorbitol accumulation under increasing salinities, and hence can be characterized as euryhaline. In contrast, the introduced Schizymenia spp. and native C. novae-zelandiae, which preferentially occur in the mid-intertidal, showed a narrower salinity tolerance. The species-specific responses reflect their respective vertical positions in the intertidal zone.