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Paralia (Bacillariophyta) stowaways in ship ballast: implications for biogeography and diversity of the genus.

MacGillivary ML, Kaczmarska I - J Biol Res (Thessalon) (2015)

Bottom Line: Frustule morphology did not segregate species, however, comparisons of sequence fragments and ITS2 secondary structures yielded a new species from North American waters, P. guyana (with four genodemes), and another widely-distributed species, P. marina.Despite this, as of 2009, P. marina was found only in Cheticamp, Nova Scotia, Canada.Second, genetic analysis readily segregated cryptic and semi-cryptic taxa of Paralia, highlighting the usefulness of the molecular approach to species recognition, e.g., in programs monitoring alien introductions.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Mount Allison University, 63B York Street, Sackville, NB E4L 1G7 Canada.

ABSTRACT

Background: The genus Paralia Heiberg is one of the most recognizable, widely distributed and commonly reported diatoms from contemporary coastal marine environments and ship ballast. Species discovery has historically been made in diatoms through the recognition of morphological discontinuities between specimens, first using light and later electron microscopy. However, recently, morphologically semi-cryptic species of Paralia were delineated using genetic analyses, among mostly tropical and subtropical sites.

Results: Ten morphological characters of the frustules and sequence fragments from the nuclear genome (conserved 18S regions of ribosomal RNA and the variable internal transcribed spacer [ITS]), and from the RuBisCo large subunit (rbcL) gene of the chloroplast genome were examined. Frustule morphology did not segregate species, however, comparisons of sequence fragments and ITS2 secondary structures yielded a new species from North American waters, P. guyana (with four genodemes), and another widely-distributed species, P. marina. The latter was lecto- and epitypified here because it is most similar to specimens in the type preparation BM1021 representing Smith's concept of the species. Paralia marina and certain genodemes of P. guyana were morphologically cryptic. Only those genodemes of P. guyana that possess prickly separation valves could be morphologically distinguished from P. marina with relative confidence in SEM preparations. All clones established from chains isolated from the ballast sediment of the ships sailing along the Atlantic coast of North America belonged to P. guyana. All DNA sequences of preserved Paralia chains recovered from the three trans-Atlantic voyages (TAVs) samples arriving to eastern Canada from Europe shared 100% identity with P. marina.

Conclusion: First, if the [Formula: see text] = 130592 P. marina cells per ballast tank at the end of the TAVs represents their abundance in ballast tanks of similar crossings and following mid-ocean ballast water exchange, then this diatom, if de-ballasted, exerts a strong and continued propagule pressure on Eastern Canadian coasts. Despite this, as of 2009, P. marina was found only in Cheticamp, Nova Scotia, Canada. Second, genetic analysis readily segregated cryptic and semi-cryptic taxa of Paralia, highlighting the usefulness of the molecular approach to species recognition, e.g., in programs monitoring alien introductions.

No MeSH data available.


Related in: MedlinePlus

Maximum likelihood (ML) tree of plastidal-encodedrbcL sequence ofParalia. The fragment used corresponded to a 540 bp barcode segment of the RuBisCo large subunit (rbcL). Stephanopyxis palmeriana is the outgroup; four clades of taxa are labelled I, II, III and IV with bootstrap support (ML/MP/NJ). Separation valve type is shown to the right of the terminal branches. The number in parentheses next to the taxon name represents the number of clones (or single chains in the case of P. fenestrata) used in construction of the tree if not all are shown (i.e., P. guyana ‘smooth’ genodeme and P. marina). Representative clones were selected based on methods used to generate Figure 10 (see text for explanation).
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Fig14: Maximum likelihood (ML) tree of plastidal-encodedrbcL sequence ofParalia. The fragment used corresponded to a 540 bp barcode segment of the RuBisCo large subunit (rbcL). Stephanopyxis palmeriana is the outgroup; four clades of taxa are labelled I, II, III and IV with bootstrap support (ML/MP/NJ). Separation valve type is shown to the right of the terminal branches. The number in parentheses next to the taxon name represents the number of clones (or single chains in the case of P. fenestrata) used in construction of the tree if not all are shown (i.e., P. guyana ‘smooth’ genodeme and P. marina). Representative clones were selected based on methods used to generate Figure 10 (see text for explanation).

Mentions: The overall topologies of the trees inferred from all the analyses (ML, MP and NJ) were similar for the 18S, ITS, concatenated nuclear 18S + 5.8S + ITS2 and rbcL marker phylogenies. Consequently, we present only the concatenated nuclear encoded (Figure 13) and plastidal rbcL trees (Figure 14). In the phylogenetic analysis of 18S + 5.8S + ITS2 three major clades were recovered with similar morphological separation as that found in the rbcL (containing larger number of species). The P. guyana clade (clade I) received stronger bootstrap support in 18S + 5.8S + ITS2 (92/88/100%, Figure 13) than in the rbcL tree (78/52/75%, Figure 14). Each genodeme of P. guyana occupied its own terminal branch in the 18S + 5.8S + ITS2 (>89%) tree whereas in the rbcL tree, the P. guyana ‘smooth’ genodeme and the three prickly genodemes of P. guyana formed common terminal groups (>92%). Support was similar for clade II in the concatenated rDNA (94/91/100%) and rbcL (96/99/95%) trees. For clade III, comprised of P. marina, similar support was shown in the 18S + 5.8S + ITS2 and rbcL trees (>97%). Paralia allisonii and P. crawfordii occupied terminal branches in clade II and had high support in both the concatenated (>92%) and rbcL (>98%) trees. The 18S + 5.8S + ITS2 sequence for P. fenestrata could not be obtained from the few single chains available; these chains were also uncultivable and so this species is absent from the concatenated tree. Nonetheless, P. fenestrata occupied a terminal branch in the rbcL tree and received poor to strong support (90/60/89%, Figure 14), depending on the analysis.Figure 13


Paralia (Bacillariophyta) stowaways in ship ballast: implications for biogeography and diversity of the genus.

MacGillivary ML, Kaczmarska I - J Biol Res (Thessalon) (2015)

Maximum likelihood (ML) tree of plastidal-encodedrbcL sequence ofParalia. The fragment used corresponded to a 540 bp barcode segment of the RuBisCo large subunit (rbcL). Stephanopyxis palmeriana is the outgroup; four clades of taxa are labelled I, II, III and IV with bootstrap support (ML/MP/NJ). Separation valve type is shown to the right of the terminal branches. The number in parentheses next to the taxon name represents the number of clones (or single chains in the case of P. fenestrata) used in construction of the tree if not all are shown (i.e., P. guyana ‘smooth’ genodeme and P. marina). Representative clones were selected based on methods used to generate Figure 10 (see text for explanation).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4389653&req=5

Fig14: Maximum likelihood (ML) tree of plastidal-encodedrbcL sequence ofParalia. The fragment used corresponded to a 540 bp barcode segment of the RuBisCo large subunit (rbcL). Stephanopyxis palmeriana is the outgroup; four clades of taxa are labelled I, II, III and IV with bootstrap support (ML/MP/NJ). Separation valve type is shown to the right of the terminal branches. The number in parentheses next to the taxon name represents the number of clones (or single chains in the case of P. fenestrata) used in construction of the tree if not all are shown (i.e., P. guyana ‘smooth’ genodeme and P. marina). Representative clones were selected based on methods used to generate Figure 10 (see text for explanation).
Mentions: The overall topologies of the trees inferred from all the analyses (ML, MP and NJ) were similar for the 18S, ITS, concatenated nuclear 18S + 5.8S + ITS2 and rbcL marker phylogenies. Consequently, we present only the concatenated nuclear encoded (Figure 13) and plastidal rbcL trees (Figure 14). In the phylogenetic analysis of 18S + 5.8S + ITS2 three major clades were recovered with similar morphological separation as that found in the rbcL (containing larger number of species). The P. guyana clade (clade I) received stronger bootstrap support in 18S + 5.8S + ITS2 (92/88/100%, Figure 13) than in the rbcL tree (78/52/75%, Figure 14). Each genodeme of P. guyana occupied its own terminal branch in the 18S + 5.8S + ITS2 (>89%) tree whereas in the rbcL tree, the P. guyana ‘smooth’ genodeme and the three prickly genodemes of P. guyana formed common terminal groups (>92%). Support was similar for clade II in the concatenated rDNA (94/91/100%) and rbcL (96/99/95%) trees. For clade III, comprised of P. marina, similar support was shown in the 18S + 5.8S + ITS2 and rbcL trees (>97%). Paralia allisonii and P. crawfordii occupied terminal branches in clade II and had high support in both the concatenated (>92%) and rbcL (>98%) trees. The 18S + 5.8S + ITS2 sequence for P. fenestrata could not be obtained from the few single chains available; these chains were also uncultivable and so this species is absent from the concatenated tree. Nonetheless, P. fenestrata occupied a terminal branch in the rbcL tree and received poor to strong support (90/60/89%, Figure 14), depending on the analysis.Figure 13

Bottom Line: Frustule morphology did not segregate species, however, comparisons of sequence fragments and ITS2 secondary structures yielded a new species from North American waters, P. guyana (with four genodemes), and another widely-distributed species, P. marina.Despite this, as of 2009, P. marina was found only in Cheticamp, Nova Scotia, Canada.Second, genetic analysis readily segregated cryptic and semi-cryptic taxa of Paralia, highlighting the usefulness of the molecular approach to species recognition, e.g., in programs monitoring alien introductions.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Mount Allison University, 63B York Street, Sackville, NB E4L 1G7 Canada.

ABSTRACT

Background: The genus Paralia Heiberg is one of the most recognizable, widely distributed and commonly reported diatoms from contemporary coastal marine environments and ship ballast. Species discovery has historically been made in diatoms through the recognition of morphological discontinuities between specimens, first using light and later electron microscopy. However, recently, morphologically semi-cryptic species of Paralia were delineated using genetic analyses, among mostly tropical and subtropical sites.

Results: Ten morphological characters of the frustules and sequence fragments from the nuclear genome (conserved 18S regions of ribosomal RNA and the variable internal transcribed spacer [ITS]), and from the RuBisCo large subunit (rbcL) gene of the chloroplast genome were examined. Frustule morphology did not segregate species, however, comparisons of sequence fragments and ITS2 secondary structures yielded a new species from North American waters, P. guyana (with four genodemes), and another widely-distributed species, P. marina. The latter was lecto- and epitypified here because it is most similar to specimens in the type preparation BM1021 representing Smith's concept of the species. Paralia marina and certain genodemes of P. guyana were morphologically cryptic. Only those genodemes of P. guyana that possess prickly separation valves could be morphologically distinguished from P. marina with relative confidence in SEM preparations. All clones established from chains isolated from the ballast sediment of the ships sailing along the Atlantic coast of North America belonged to P. guyana. All DNA sequences of preserved Paralia chains recovered from the three trans-Atlantic voyages (TAVs) samples arriving to eastern Canada from Europe shared 100% identity with P. marina.

Conclusion: First, if the [Formula: see text] = 130592 P. marina cells per ballast tank at the end of the TAVs represents their abundance in ballast tanks of similar crossings and following mid-ocean ballast water exchange, then this diatom, if de-ballasted, exerts a strong and continued propagule pressure on Eastern Canadian coasts. Despite this, as of 2009, P. marina was found only in Cheticamp, Nova Scotia, Canada. Second, genetic analysis readily segregated cryptic and semi-cryptic taxa of Paralia, highlighting the usefulness of the molecular approach to species recognition, e.g., in programs monitoring alien introductions.

No MeSH data available.


Related in: MedlinePlus