Origins of Algae and their Plastids

290 Pages·1997·8.52 MB·English

by  Debashish Bhattacharya (auth.)

Debashish Bhattacharya (ed.)
Origins of AIgae and their Plastids
Plant Systematics and Evolution
Supplement Il
Springer-V erlag Wien GmbH
Dr DEBASHISH BHATTACHARYA
University of Iowa, Department of Biological Sciences, Iowa City, United States
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© 1997 Springer-Verlag Wien
Originally published by Springer-Verlag Wien New York 1997
Typesetting: Thomson Press (India) Ltd., New Delhi
Graphic design: Ecke Bonk
Printed on acid-free and chlorine-free bleached paper
SPIN: 10632388
With 55 Figures
CIP data applied for
ISSN 0172-6668
ISBN 978-3-211-83035-2 ISBN 978-3-7091-6542-3 (eBook)
DOI 10.1007/978-3-7091-6542-3
Preface
The algae are photosynthetic eukaryotes that include the dominant primary
producers on our planet. Research in the past ten years using molecular
evolutionary methods has led to many important insights that have fundamentally
changed our view of algal origin and phylogeny. This book reports on this dynamic
period of research by dealing in separate chapters with the significant advances in
each of the major algal lineages. It is my hope that these data will convince readers
not familiar with algal evolution that the origin of this group constitutes one of the
most interesting aspects of biology. It is also my hope that the phylogenies shown
in the following chapters will not only be further tested, added to, and refined by
the respective authors and others interested in those groups but that the trees will be
used to formulate deeper questions about cellular and genetic evolution. The most
important role of molecular phylogenetics is not to underpin certain hypotheses
that arise from tree topologies but to present trees as experimental tools for a better
understanding of the evolution of organisms.
In organizing this special supplement, I have asked, as much as possible, young
researchers to provide their data and perspectives on algal phylogeny and
evolution. I am grateful to those authors and to their mentors for making the book
possible. In addition I thank Prof. EHRENDORFER who gave me the chance to
organize this volume as well as SILVIA SCHILGERIUS at Springer-Wien for her help
and especially Dr IRMGARD KRISAI-GREILHUBER (University of Wien) who acted as
the second reviewer of the manuscripts.
September 29, 1997 Debashish Bhattacharya
Contents
List of Contributors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IX
BHATTACHARYA, D.: An introduction to algal phylogeny and phylogenetic
methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
TURNER, S.: Molecular systematics of oxygenic photosynthetic bacteria. . . 13
DELWICHE, C. E, PALMER, J. D.: The origin of plastids and their spread via
secondary symbiosis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
FRIEDL, T.: The evolution of the Green Algae. . . . . . . . . . . . . . . . . . . . . 87
Huss, V. A. R, KRANZ, H. D.: Charophyte evolution and the origin
of land plants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 103
SAUNDERS, G. W., KRAFT, G. T.: A molecular perspective on red algal
evolution: focus on the Florideophycidae . . . . . . . . . . . . . . . . . . . .. 115
BHATTACHARYA, D., SCHMIDT, H. A.: Division Glaucocystophyta. . . . . . . .. 139
LbFFELHARDT, W., BOHNERT, H. J., BRYANT, D. A.: The complete sequence
of the Cyanophora paradoxa cyanelle genome (Glaucocystophyceae) 149
FRAUNHOLZ, M. J., WASTL, J., ZAUNER, S., RENSING, S. A., SCHERZINGER,
M. M., MAIER, u.-G.: The evolution of cryptophytes . . . . . . . . . . . .. 163
McFADDEN, G. I., GILSON, P. R, HOFMANN, C. J. B.:
Division Chlorarachniophyta. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 175
MEDLIN, L. K., KOOISTRA, W. H. C. E, POTTER, D., SAUNDERS, G. W.,
ANDERSEN, R A.: Phylogenetic relationships of the 'golden algae'
(haptophytes, heterokont chromophytes) and their plastids. . . . . . . . .. 187
DRUEHL, L. D., MAYES, c., TAN, I. R., SAUNDERS, G. W.: Molecular
and morphological phylogenies of kelp and associated brown algae .. 221
SAUNDERS, G. W., HILL, D. R A., SEXTON, J. P., ANDERSEN, R A.:
Small-subunit ribosomal RNA sequences from selected dinoflagellates:
testing classical evolutionary hypotheses with molecular systematic
methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 237
McFADDEN, G. I., WALLER, R. E, REITH, M. E., LANG-UNNASCH, N.:
Plastids in apicomplexan parasites . . . . . . . . . . . . . . . . . . . . . . . . .. 261
Listed in Current Contents
List of Contributors
ROBERT A. ANDERSEN, Bigelow Laboratory for Ocean Sciences, West Boothbay
Harbor, Maine 04575, USA
DEBASHISH BHATTACHARYA, University of Iowa, Department of Biological Science,
Biology Building, Iowa City 52242-1324, Iowa, USA (e-mail: dbhattac@blue.
weeg.uiowa.edu)
H. J. BOHNERT, Department of Biochemistry, University of Arizona, Tucson, AZ
85721, USA
D. A. BRYANT, Department of Biochemistry and Molecular Biology, The
Pennsylvania State University, University Park, PA 16802, USA
CHARLES F. DELWICHE, Department of Plant Biology, University of Maryland,
College Park, MD 20742, USA
L. D. DRUEHL, Barnfield Marine Station, Barnfield, B. C. Canada VOH IBO
MARTIN FRAUNHOFER, UniversiHit Marburg, Zellbiologie, Karl-von-Frisch-Strasse,
D-35032 Marburg, Federal Republic of Germany
THOMAS FRIEDL, Fachbereich Biologie, Allgemeine Botanik, Universitat Kaisers
lautern, Postfach 3049, D-67653 Kaiserslautern, Federal Republic of Germany,
(fax: [phone]; e-mail: [email protected])
PAUL R. GILSON, Plant Cell Biology Research Centre, School of Botany, University
of Melbourne, Parkville 3052, Australia
D. R. A. HILL, School of Botany, University of Melbourne, Parkville, Victoria
3052, Australia
CLAUDIA J. B. HOFMANN, Lehrstuhl fur Pftanzensystematik, Universitat Bayreuth, D-
95440 Bayreuth, Federal Republic of Germany
VOLKER A. R. Huss, Institut fUr Botanik und Pharmazeutische Biologie der
Universitat, Staudtstrasse 5, D-91058 Erlangen, Federal Republic of Germany
WIEBE H. C. F. KOOISTRA, NAOS Smithsonian Tropical Research Institute, APO AA
34002 0948, USA
G. T. KRAFT, School of Botany, University of Melbourne, Parkville, Victoria 3052,
Australia
HARALD D. KRANZ, Max-Planck-Institut fUr Zuchtungsforschung, Abteilung
Biochemie, Carl-von-Linne-Weg 10, D-50829 Kaln, Federal Republic of Germany
NAOMI LANG-UNNASCH, Division of Geographic Medicine, Department of Medicine,
University of Alabama at Birmingham, Birmingham, Alabama 35294-2170, USA
x List of contributors
W. LOFFELHARDT, Institut fUr Biochemie und Molekulare Zellbiologie der
UniversiHit Wien und Ludwig-Boltzmann-Forschungsstelle fUr Biochemie. Dr.
Bohrgasse, 9, A-I030 Vienna, Austria
UWE-G. MAIER, UniversiHit Marburg, Zellbiologie, Karl-von-Frisch-Strasse, D-
35032 Marburg, Federal Republic of Germany
c.,
C. MAYES, Biological Sciences, Simon Fraser University, Burnaby, B. Canada
V5A IS6
GEOFFREY I. McFADDEN, Plant Cell Biology Research Centre, School of Botany,
University of Melbourne, Parkville 3052, Australia
LINDA K. MEDLIN, Alfred-Wegener-Institute, Am Handelshafen 12, D-27570
Bremerhaven, Germany
JEFFREY D. PALMER, Department of Biology, Indiana University, Bloomington, IN
47405, USA
DANIEL POTTER, Department of Pomology, University of California, Davis 95616,
USA
MICHAEL E. REITH, Institute for Marine Biosciences, National Research Council,
1411 Oxford St, Halifax B3H 3ZI, NS, Canada
STEFAN A. RENSING, UniversiHit Freiburg, Lehrstuhl fUr Zellbiologie, Schanzle
strasse I, D-79104 Freiburg, Federal Republic of Germany
G. W. SAUNDERS, Department of Biology, University of New Brunswick,
Fredericton, N. B., Canada, E3B 6El
MARGITTA M. SCHERZINGER, Universitat Freiburg, Lehrstuhl fUr Zellbiologie,
Schanzlestrasse I, D-79104 Freiburg, Federal Republic of Germany
HEIKO A. SCHMIDT, Deutsches Krebsforschungszentrum, Theoretische Bioinforma
tik (815), 1m Neuenheimer Feld 280, D-69120 Heidelberg, Federal Republic of
Germany
J. P. SEXTON, Bigelow Laboratory for Ocean Sciences, West Boothbay Harbor, ME
04575, USA
I. H. TAN, Biological Sciences, Simon Fraser University, Burnaby, B. C., Canada
V5A IS6
SEAN TURNER, Department of Biology, Jordan Hall 142, Indiana University,
Bloomington, Indiana 47405, USA (e-mail: [email protected])
Ross F. WALLER, Plant Cell Biology Research Centre, School of Botany, University
of Melbourne, VIC 3052, Australia
JDRGEN WASTL, Universitat Marburg, Zellbiologie, Karl-von-Frisch-Strasse, D-
35032 Marburg, Federal Republic of Germany
STEFAN ZAUNER, Universitat Marburg, Zellbiologie, Karl-von-Frisch-Strasse, D-
35032 Marburg, Federal Republic of Germany
-Plant'-.--
SystematIcs
PI. Syst. Evoi. [SuppI.] 11: 1-11 (1997)
and
Evolution
© Springer-Verlag 1997
An introduction to algal phylogeny
and phylogenetic methods
DEBASHISH BHATTACHARYA
Key words: Algae. - Endosymbiosis, evolution, phylogeny, plastids, systematics,
taxonomy.
Abstract: The algae are an assemblage of morphologically diverse, photosynthetic protists
that are Ubiquitous in distribution. The understanding of algal phylogeny has been
revolutionized with molecular evolutionary methods. These analyses have shown that the
algae are of a polyphyletic origin and diverge nearly simultaneously from each other in the
crown group radiation (except euglenophytes). An interesting perspective on algal origin is
gained by the analysis of plastid origin because many plastids (e.g., in cryptophytes,
dinoflagellates, chlorarachniophytes, and euglenophytes) have arisen multiple, independent
times through secondary endosymbioses. This chapter is an introduction to algal phylogeny
and to the most common methods used in the construction of evolutionary trees. The
subsequent 13 chapters in this book deal with specific aspects of the phylogeny of
cyanobacteria (the primary source of the algal plastid), plastids and all the major algal
lineages.
The striking morphology of many micro- and macroalgae (e.g., desmids, kelps) has
often been sufficient reason for many scientists to engage in phycological research.
Algae have played central roles in ecological studies of aquatic and terrestrial
ecosystems, been used as "model" protists in physiological and biochemical
studies and in reconstructing and predicting climate change, and have posed many
fundamental questions in biology due to their diverse and complex life histories
(BOLD & WYNNE 1985). Algae have also had a long history in the food (e.g., nori,
wakame) and pharmaceutical (e.g., agar-agar, carrageenan, alginic acid) industries.
Studies of algal systematics have led to the description of thousands of taxa (5000-
5500 species in the Rhodophyta alone, VAN DEN HOEK & al. 1993) to aid in their
taxonomic classification and further the understanding of their origins and
evolutionary relationships.
Many of these studies, using "traditional" markers of species relationships,
such as gross morphology or vegetative and reproductive cell ultrastructure (KIES
1974, STEWART & MATTOX 1975, TAYLOR 1976, MOESTRUP 1978, KRAFr 1981,
CAVALIER-SMITH 1982, O'KELLY 1992), have allowed a deeper understanding of the
uniqueness and complexity of algal cells and lineages and the phylogeny of
members within these lineages. Traditional phylogenetics has not, however, proven
to be very powerful in uncovering the relationships of algae with other eukaryotes
2 D. BHATTACHARYA:
(glaucocystophytes, see chapter 7 of this volume; chlorarachniophytes, chapter 10;
dinoflagellates, chapter 13). One problem arises from the difficulties in assigning
phylogenetic value to certain key characters (e.g., ultrastructure of flagellar hairs)
in distantly related groups that either vary substantially in morphology and are of
questionable homology (found in the common ancestor of a group) or seem to be
homologous but may have arisen from convergence (independently evolved in
different groups). Another potential problem comes from the use of plastid
characters to define host cell lineages and to infer relationships among them (see
below). A great advantage of modem phylogenetic methods using protein or
nucleotide sequence comparisons is that they offer the possibility to arrange
species in natural groups independent of their morphology. Such analyses have
revolutionized the field of algal evolution by providing insights into the
phylogenetic position of algae in the larger eukaryotic phylogeny and insights
into the origin of the key morphological characters that define these clades
(CAVALIER-SMITH 1993, FRESHWATER & al. 1994, SCHLEGEL 1994, BHATTACHARYA &
MEDLIN 1995, PALMER & DELWICHE 1996).
Goals of this book
The main goal of this book is to provide the current results and hypotheses
regarding the origins of the algae and their plastids (photosynthetic organelles)
using gene/protein sequence comparisons. The sequence analyses should be
interpreted in terms of phylogeny ("The evolutionary history of a group of taxa or
genes and their ancestors", LI & GRAUR 1991: 244) and not necessarily taxonomy
("The principles and procedures according to which species are named and
assigned to taxonomic groups", LI & GRAUR 1991: 250). Though molecular
sequence data may be interpreted to create new or confirm existing taxonomic
schemes there is no a priori reason why this has to be done. The connection
between phylogeny and taxonomy remains a highly controversial area in biology
and does not form the main focus of this book.
The wealth of phylogenetic data regarding the evolutionary relationships of
algal groups that have been published in the past 5-6 years show that the algae are
of polyphyletic origins (reviewed in BHATTACHARYA & MEDLIN 1995). The algae
comprise multiple, often distantly related (e.g., euglenophytes, heterokonts,
dinoflagellates) lineages that are synthetically grouped on the basis of
photosynthetic capacity. Many algal lineages, for example the euglenophytes and
chlorarachniophytes, share a closer phylogenetic relationship with non-algal taxa
(kinetoplastids and filose amoebae, respectively) than with other photosynthetic
eukaryotes.
The understanding of plastid endosymbiosis (the accepted theory for the origin
of the plastid; MERESCHKOWSKI 1905, 1910; MARGULIS 1981) is critical for the
understanding of algal origin (s) since plastids have been laterally transferred
multiple times in algal evolution. Resolution of plastid origins has been greatly
advanced by the recent availability of plastid sequence data (or complete genome
sequences, REITH & MUNHOLLAND 1995, KOWALLIK & al. 1995; HALLICK & al. 1993,
LOFFELHARDT & al. 1996) from all the major algal groups for comparative analyses.
These data are, in general, consistent with the hypothesis that the origin of all algal
Algal evolution 3
plastids can be traced to a single primary endosymbiosis (CAVALIER-SMITH 1982,
BHATTACHARYA & MEDLIN 1995, PALMER & DELWICHE 1996) involving a coccoid
cyanobacterium and a nonphotosynthetic free-living unicellular eukaryote. This
"proto-alga" had two plastid bounding membranes. The origins of all algae
cannot, however, be directly traced to a unique common ancestor. Many algae that
contain plastids with more than two bounding-membranes have derived their
photosynthetic capacity from the engulfment of an existing alga (e.g., heterokonts,
chlorarachniophytes, euglenophytes-secondary endosymbiosis; GIBBS 1993; see
also chapters 9, 10, 11). In some cases there is evidence that a plastid of a
secondary endosymbiotic origin replaced an existing plastid of a primary
endosymbiotic origin (see chapter 9). Algal and plastid origins may therefore be
dealt with as interdependent topics because plastid lateral transfer via secondary
endosymbiosis has in many cases transformed a previously nonphotosynthetic
protist into an "alga".
For these reasons resolution of the processes of primary and secondary
endosymbioses that have resulted in the origin of algal plastids continues to be one
of the most interesting (and disputed) problems in biology (see DOUGLAS & TURNER
1991, MARTIN & al. 1992, MORDEN & al. 1992, LOISEAUX-DE-GbER 1994,
BHATTACHARYA & MEDLIN 1995) and forms a major focus of this book (e.g.,
chapters 2, 3, 7, 8). The most common "for" and "against" theories regarding
plastid origins involve those who support fewer endosymbiotic events (both
primary and secondary) as explanation for the origin of all plastids (e.g., CAVALIER
SMITH 1982) and those who favor a greater number of events (e.g., RAVEN 1970,
MARGULIS 1981, WHATLEY 1993). Support for either theory is often tied with
assumptions regarding secondary plastid loss (or plastid replacement), a
phenomenon that is not yet well understood in algal evolution.
Molecular markers
The small subunit coding region of ribosomal DNA (SSU rDNA) is the most
common molecular marker currently used in phylogenetic reconstruction. The
eukaryotic nuclear encoded rDNA genes are encoded in an operon (SSU-5.8S
LSU) that normally exists as multicopy tandem repeats. Strong concerted evolution
resulting from unequal crossing-over and/or gene conversion (see DOVER 1982)
results in the homogenization of all gene copies so that the entire gene family is
normally represented by a unique copy of each coding region (for exceptions, see
MCCUTCHAN & al. 1988, SCHOLIN & al. 1993). The small and large subunit coding
region of the rDNAs exist within all living organisms (excluding phages/viruses)
and these molecules share enough sequence conservation that a satisfactory
alignment for phylogenetic analyses can be created that includes eukaryotes,
eubacteria and archaebacteria. There are, however, also less well conserved and
highly variable regions in rDNA that can be used to resolve the phylogeny of more
closely related taxa.
That rRNA secondary structure is also highly conserved facilitates greatly the
alignment of homologous regions from distantly related taxa (SOGIN & al. 1989,
MAIDAK & al. 1994, VAN DE PEER & al. 1996a). Further characteristics and
advantages offered by SSU rDNA as a molecular marker include a relatively large