DOCSLIB.ORG

Molecular Phylogeny of Choanoflagellates, the Sister Group to Metazoa

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Molecular Phylogeny of Choanoflagellates, the Sister Group to Metazoa Molecular phylogeny of choanoflagellates, the sister group to Metazoa M. Carr*†, B. S. C. Leadbeater*‡, R. Hassan‡§, M. Nelson†, and S. L. Baldauf†¶ʈ †Department of Biology, University of York, Heslington, York, YO10 5YW, United Kingdom; and ‡School of Biosciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT, United Kingdom Edited by Andrew H. Knoll, Harvard University, Cambridge, MA, and approved August 28, 2008 (received for review February 28, 2008) Choanoflagellates are single-celled aquatic flagellates with a unique family. Members of the Acanthoecidae family (Norris 1965) are morphology consisting of a cell with a single flagellum surrounded by characterized by the most distinct periplast morphology. This a ‘‘collar’’ of microvilli. They have long interested evolutionary biol- consists of a complex basket-like lorica constructed in a precise and ogists because of their striking resemblance to the collared cells highly reproducible manner from ribs (costae) composed of rod- (choanocytes) of sponges. Molecular phylogeny has confirmed a close shaped silica strips (Fig. 1 E and F) (13). The Acanthoecidae family relationship between choanoflagellates and Metazoa, and the first is further subdivided into nudiform (Fig. 1E) and tectiform (Fig. 1F) choanoflagellate genome sequence has recently been published. species, based on the morphology of the lorica, the stage in the cell However, molecular phylogenetic studies within choanoflagellates cycle when the silica strips are produced, the location at which the are still extremely limited. Thus, little is known about choanoflagel- strips are stored, and the mode of cell division [supporting infor- late evolution or the exact nature of the relationship between mation (SI) Text] (14). choanoflagellates and Metazoa. We have sequenced four genes from Speculation on a possible close evolutionary relationship be- a broad sampling of the morphological diversity of choanoflagellates tween choanoflagellates and Metazoa was strengthened early on by including most species currently available in culture. Phylogenetic the discovery of a colonial choanoflagellate, Proterospongia haeck- analyses of these sequences, alone and in combination, reject much eli, by Saville-Kent in 1880. This taxon superficially resembles a of the traditional taxonomy of the group. The molecular data also poriferan larva in that it appears to consist of flagellated cells strongly support choanoflagellate monophyly rejecting proposals protruding from a matrix bearing internal amoeboid-like cells (11). that Metazoa were derived from a true choanoflagellate ancestor. Although subsequent sightings of this species have not been au- Mapping of a complementary matrix of morphological and ecological thenticated, and its original description is somewhat enigmatic, traits onto the phylogeny allows a reinterpretation of choanoflagel- numerous other colonial forms are now known. Thus, cho- late character evolution and predicts the nature of their last common anoflagellates have long been treated in introductory biology texts ancestor. as a classic example of stepwise evolution of complexity leading to the true multicellularity of Metazoa. evolution ͉ morphology ͉ holozoa ͉ animals ͉ protists Most molecular phylogenetic trees that include multiple cho- anoflagellate species have been based on nuclear small subunit, EVOLUTION hoanoflagellates are a major group of heterotrophic ribosomal gene (SSU rDNA) sequences. These studies have mostly Cnanoflagellates, ubiquitously distributed in aquatic environ- recovered choanoflagellate monophyly but have been hampered by ments (1). These single-celled organisms were first described by a small sampling of species and some species misidentification (4–5, James-Clark in 1866, who was also the first to note the strong 7–9). Therefore, to examine major trends in choanoflagellate resemblance between the choanoflagellate cell morphology and evolution, we have constructed a taxonomically broad, multigene that of the collared cells (choanocytes) of sponges (Porifera) (2). phylogeny of the group and a complementary matrix of morpho- Based on these similarities, a close relationship between cho- logical and ecological traits. Phylogenetic analyses of a concate- anoflagellates and Metazoa was long postulated and has now been nated four-gene dataset show that the traditional taxonomy of confirmed (3–9). However, there is still very little molecular data choanoflagellates is flawed, and the evolution of some of their most from more than two or three choanoflagellate species. Thus, we notable morphological traits is more complex than initially thought. have a limited understanding of choanoflagellate phylogeny or how Results to interpret evolutionary trends within the group. Most importantly, without knowing whether choanoflagellates constitute a monophy- Molecular Phylogeny of Choanoflagellates. Large fragments of the letic group, it is difficult to know the relevance of such trends to the nuclear SSU and large subunit (LSU) ribosomal RNA, alpha- early evolution of Metazoa. tubulin (tubA), and the 90-kDa heat shock protein (hsp90) coding Choanoflagellates are characterized by a distinctive and re- markably uniform cell body (protoplast) morphology. This com- Author contributions: M.C., B.S.C.L., and S.L.B. designed research; M.C., R.H., and M.N. prises a spherical to ovoid cell with a single anterior flagellum performed research; M.C., B.S.C.L., and S.L.B. analyzed data; M.C., B.S.C.L., and S.L.B. wrote surrounded by a collar of narrow actin-based microvilli (Fig. 1A) the paper. (10). In contrast to the uniformity of the choanoflagellate cell, The authors declare no conflict of interest. the morphology of the external covering (periplast) is varied and This article is a PNAS Direct Submission. sometimes striking, ranging from simple organic sheaths to Data Deposition: Sequences reported in this paper have been deposited in the GenBank complex silica ‘‘cages’’ up to a 100 ␮m or more in length. database (accession numbers EU011922–EU011972). Periplast morphology has formed the basis of the conventional ʈTo whom correspondence should be addressed. E-mail: [email protected]. classification of choanoflagellates into three families (11). Members §Present address: Department of Aquatic Sciences, Faculty of Resource Science and Tech- of the Codonosigidae family (Kent 1880) (Fig. 1A) have a thin nology, Universiti Malaysia Sarawak, Malaysia. fibrillar coat, the glycocalyx. This surrounds the cell and may extend ¶Present address: Department of Evolution, Genomics and Systematics, Evolutionary Biol- posteriorly to join a substantial stalk composed of carbohydrate ogy Centre, Uppsala University, Norbyva¨gen 18D, 752–36 Uppsala, Sweden. microfibrils (12). Species of the Salpingoecidae family (Kent 1880) *M.C. and B.S.C.L. contributed equally to this work. possess a substantial microfibril-based theca. This may be flask- This article contains supporting information online at www.pnas.org/cgi/content/full/ (Fig. 1B), cup- (Fig. 1C) or tube-shaped and is attached to the 0801667105/DCSupplemental. substratum by a stalk similar to that found in the Codonosigidae © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0801667105 PNAS ͉ October 28, 2008 ͉ vol. 105 ͉ no. 43 ͉ 16641–16646 Downloaded by guest on September 25, 2021 f c c Fig. 1. Morphological variation within cho- anoflagellates. Shadowcast whole mounts of cells or thecae viewed with transmission elec- tron microscopy. (A) Monosiga ovata. (c) col- lar; f, flagellum. Bar ϭ 2 ␮m. (B) Salpingoeca p urceolata. Empty flask-shaped theca is shown. Arrow denotes inner flange that con- AB Cnects cell (absent) to theca. (Scale bar, 1 ␮m.) (C) Salpingoeca infusionum. Empty cup- f shaped organic theca is shown. (p) peduncle ␮ f (stalk). (Scale bar, 1 m.) (D) Salpingoeca am- phoridium. Colonial ‘‘proterospongia’’ stage is shown. Note six regularly placed cells held together by fine posterior threads. (Scale bar, 5 ␮m.) (E) Acanthoeca spectabilis. Immedi- ately after division (nudiform) showing two cells, each with a forwardly directed flagel- lum (arrows in F) is shown. The juvenile (j) is above the cell remaining in the parent lorica. (Scale bar, 2 ␮m.) (F) Stephanoeca diplo- costata. Tectiform division showing inverted juvenile cell (j) being pushed into an accumu- lation of costal stripsis shown. Arrows denote DE Ftransverse (ring) costae. (Scale bar, 2 ␮m.) genes were amplified by PCR from total genomic DNA for 16 (assigned to Clades 1 and 2, respectively). Within Clade 3, the two choanoflagellate species (Table S1). SSU rDNA was sequenced major morphological types of acanthoeicids, nudiform, and tecti- directly from PCR products for all species, from which no evidence form, are both recovered as strongly supported monophyletic of polymorphism was detected. LSU rRNA and both protein genes subgroups (1.00 biPP, 89–100% mlBP) (Fig. 2). This is particularly were amplified in multiple overlapping fragments, all of which significant with respect to the morphologically disparate nudiform matched completely in overlapping regions. Thus, there is no species for it demonstrates that they are an evolutionarily coherent evidence for the existence of paralogs for any of these genes in any assemblage. of the examined species. Two colony-forming Proterospongia species are found in Clade 1, Phylogenetic analyses of each of the four genes independently although they do not group together, whereas a third colony- show similar results for each gene
Load more

Recommended publications
  • A Six-Gene Phylogeny Provides New Insights Into Choanoflagellate Evolution Martin Carr, Daniel J
    A six-gene phylogeny provides new insights into choanoflagellate evolution Martin Carr, Daniel J. Richter, Parinaz Fozouni, Timothy J. Smith, Alexandra Jeuck, Barry S.C. Leadbeater, Frank Nitsche To cite this version: Martin Carr, Daniel J. Richter, Parinaz Fozouni, Timothy J. Smith, Alexandra Jeuck, et al.. A six- gene phylogeny provides new insights into choanoflagellate evolution. Molecular Phylogenetics and Evolution, Elsevier, 2017, 107, pp.166 - 178. 10.1016/j.ympev.2016.10.011. hal-01393449 HAL Id: hal-01393449 https://hal.archives-ouvertes.fr/hal-01393449 Submitted on 7 Nov 2016 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Molecular Phylogenetics and Evolution 107 (2017) 166–178 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev A six-gene phylogeny provides new insights into choanoflagellate evolution ⇑ Martin Carr a, ,1, Daniel J. Richter b,1,2, Parinaz Fozouni b,3, Timothy J. Smith a, Alexandra Jeuck c, Barry S.C. Leadbeater d, Frank Nitsche c a School of Applied Sciences, University of Huddersfield, Huddersfield HD1 3DH, UK b Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720-3200, USA c University of Cologne, Biocentre, General Ecology, Zuelpicher Str.
    [Show full text]
  • Download This Publication (PDF File)
    PUBLIC LIBRARY of SCIENCE | plosgenetics.org | ISSN 1553-7390 | Volume 2 | Issue 12 | DECEMBER 2006 GENETICS PUBLIC LIBRARY of SCIENCE www.plosgenetics.org Volume 2 | Issue 12 | DECEMBER 2006 Interview Review Knight in Common Armor: 1949 Unraveling the Genetics 1956 An Interview with Sir John Sulston e225 of Human Obesity e188 Jane Gitschier David M. Mutch, Karine Clément Research Articles Natural Variants of AtHKT1 1964 The Complete Genome 2039 Enhance Na+ Accumulation e210 Sequence and Comparative e206 in Two Wild Populations of Genome Analysis of the High Arabidopsis Pathogenicity Yersinia Ana Rus, Ivan Baxter, enterocolitica Strain 8081 Balasubramaniam Muthukumar, Nicholas R. Thomson, Sarah Jeff Gustin, Brett Lahner, Elena Howard, Brendan W. Wren, Yakubova, David E. Salt Matthew T. G. Holden, Lisa Crossman, Gregory L. Challis, About the Cover Drosophila SPF45: A Bifunctional 1974 Carol Churcher, Karen The jigsaw image of representatives Protein with Roles in Both e178 Mungall, Karen Brooks, Tracey of various lines of eukaryote evolution Splicing and DNA Repair Chillingworth, Theresa Feltwell, refl ects the current lack of consensus as Ahmad Sami Chaouki, Helen K. Zahra Abdellah, Heidi Hauser, to how the major branches of eukaryotes Salz Kay Jagels, Mark Maddison, fi t together. The illustrations from upper Sharon Moule, Mandy Sanders, left to bottom right are as follows: a single Mammalian Small Nucleolar 1984 Sally Whitehead, Michael A. scale from the surface of Umbellosphaera; RNAs Are Mobile Genetic e205 Quail, Gordon Dougan, Julian Amoeba, the large amoeboid organism Elements Parkhill, Michael B. Prentice used as an introduction to protists for Michel J. Weber many school children; Euglena, the iconic Low Levels of Genetic 2052 fl agellate that is often used to challenge Soft Sweeps III: The Signature 1998 Divergence across e215 ideas of plants (Euglena has chloroplasts) of Positive Selection from e186 Geographically and and animals (Euglena moves); Stentor, Recurrent Mutation Linguistically Diverse one of the larger ciliates; Cacatua, the Pleuni S.
    [Show full text]
  • The Closest Unicellular Relatives of Animals
    View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Current Biology, Vol. 12, 1773–1778, October 15, 2002, 2002 Elsevier Science Ltd. All rights reserved. PII S0960-9822(02)01187-9 The Closest Unicellular Relatives of Animals B.F. Lang,1,2 C. O’Kelly,1,3 T. Nerad,4 M.W. Gray,1,5 Results and Discussion and G. Burger1,2,6 1The Canadian Institute for Advanced Research The evolution of the Metazoa from single-celled protists Program in Evolutionary Biology is an issue that has intrigued biologists for more than a 2 De´ partement de Biochimie century. Early morphological and more recent ultra- Universite´ de Montre´ al structural and molecular studies have converged in sup- Succursale Centre-Ville porting the now widely accepted view that animals are Montre´ al, Que´ bec H3C 3J7 related to Fungi, choanoflagellates, and ichthyosporean Canada protists. However, controversy persists as to the spe- 3 Bigelow Laboratory for Ocean Sciences cific evolutionary relationships among these major P.O. Box 475 groups. This uncertainty is reflected in the plethora of 180 McKown Point Road published molecular phylogenies that propose virtually West Boothbay Harbor, Maine 04575 all of the possible alternative tree topologies involving 4 American Type Culture Collection Choanoflagellata, Fungi, Ichthyosporea, and Metazoa. 10801 University Boulevard For example, a monophyletic MetazoaϩChoanoflagel- Manassas, Virginia 20110 lata group has been suggested on the basis of small 5 Department of Biochemistry subunit (SSU) rDNA sequences [1, 6, 7]. Other studies and Molecular Biology using the same sequences have allied Choanoflagellata Dalhousie University with the Fungi [8], placed Choanoflagellata prior to the Halifax, Nova Scotia B3H 4H7 divergence of animals and Fungi [9], or even placed Canada them prior to the divergence of green algae and land plants [10].
    [Show full text]
  • Sex Is a Ubiquitous, Ancient, and Inherent Attribute of Eukaryotic Life
    PAPER Sex is a ubiquitous, ancient, and inherent attribute of COLLOQUIUM eukaryotic life Dave Speijera,1, Julius Lukešb,c, and Marek Eliášd,1 aDepartment of Medical Biochemistry, Academic Medical Center, University of Amsterdam, 1105 AZ, Amsterdam, The Netherlands; bInstitute of Parasitology, Biology Centre, Czech Academy of Sciences, and Faculty of Sciences, University of South Bohemia, 370 05 Ceské Budejovice, Czech Republic; cCanadian Institute for Advanced Research, Toronto, ON, Canada M5G 1Z8; and dDepartment of Biology and Ecology, University of Ostrava, 710 00 Ostrava, Czech Republic Edited by John C. Avise, University of California, Irvine, CA, and approved April 8, 2015 (received for review February 14, 2015) Sexual reproduction and clonality in eukaryotes are mostly Sex in Eukaryotic Microorganisms: More Voyeurs Needed seen as exclusive, the latter being rather exceptional. This view Whereas absence of sex is considered as something scandalous for might be biased by focusing almost exclusively on metazoans. a zoologist, scientists studying protists, which represent the ma- We analyze and discuss reproduction in the context of extant jority of extant eukaryotic diversity (2), are much more ready to eukaryotic diversity, paying special attention to protists. We accept that a particular eukaryotic group has not shown any evi- present results of phylogenetically extended searches for ho- dence of sexual processes. Although sex is very well documented mologs of two proteins functioning in cell and nuclear fusion, in many protist groups, and members of some taxa, such as ciliates respectively (HAP2 and GEX1), providing indirect evidence for (Alveolata), diatoms (Stramenopiles), or green algae (Chlor- these processes in several eukaryotic lineages where sex has oplastida), even serve as models to study various aspects of sex- – not been observed yet.
    [Show full text]
  • Old Woman Creek National Estuarine Research Reserve Management Plan 2011-2016
    Old Woman Creek National Estuarine Research Reserve Management Plan 2011-2016 April 1981 Revised, May 1982 2nd revision, April 1983 3rd revision, December 1999 4th revision, May 2011 Prepared for U.S. Department of Commerce Ohio Department of Natural Resources National Oceanic and Atmospheric Administration Division of Wildlife Office of Ocean and Coastal Resource Management 2045 Morse Road, Bldg. G Estuarine Reserves Division Columbus, Ohio 1305 East West Highway 43229-6693 Silver Spring, MD 20910 This management plan has been developed in accordance with NOAA regulations, including all provisions for public involvement. It is consistent with the congressional intent of Section 315 of the Coastal Zone Management Act of 1972, as amended, and the provisions of the Ohio Coastal Management Program. OWC NERR Management Plan, 2011 - 2016 Acknowledgements This management plan was prepared by the staff and Advisory Council of the Old Woman Creek National Estuarine Research Reserve (OWC NERR), in collaboration with the Ohio Department of Natural Resources-Division of Wildlife. Participants in the planning process included: Manager, Frank Lopez; Research Coordinator, Dr. David Klarer; Coastal Training Program Coordinator, Heather Elmer; Education Coordinator, Ann Keefe; Education Specialist Phoebe Van Zoest; and Office Assistant, Gloria Pasterak. Other Reserve staff including Dick Boyer and Marje Bernhardt contributed their expertise to numerous planning meetings. The Reserve is grateful for the input and recommendations provided by members of the Old Woman Creek NERR Advisory Council. The Reserve is appreciative of the review, guidance, and council of Division of Wildlife Executive Administrator Dave Scott and the mapping expertise of Keith Lott and the late Steve Barry.
    [Show full text]
  • Multigene Eukaryote Phylogeny Reveals the Likely Protozoan Ancestors of Opis- Thokonts (Animals, Fungi, Choanozoans) and Amoebozoa
    Accepted Manuscript Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opis- thokonts (animals, fungi, choanozoans) and Amoebozoa Thomas Cavalier-Smith, Ema E. Chao, Elizabeth A. Snell, Cédric Berney, Anna Maria Fiore-Donno, Rhodri Lewis PII: S1055-7903(14)00279-6 DOI: http://dx.doi.org/10.1016/j.ympev.2014.08.012 Reference: YMPEV 4996 To appear in: Molecular Phylogenetics and Evolution Received Date: 24 January 2014 Revised Date: 2 August 2014 Accepted Date: 11 August 2014 Please cite this article as: Cavalier-Smith, T., Chao, E.E., Snell, E.A., Berney, C., Fiore-Donno, A.M., Lewis, R., Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa, Molecular Phylogenetics and Evolution (2014), doi: http://dx.doi.org/10.1016/ j.ympev.2014.08.012 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. 1 1 Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts 2 (animals, fungi, choanozoans) and Amoebozoa 3 4 Thomas Cavalier-Smith1, Ema E. Chao1, Elizabeth A. Snell1, Cédric Berney1,2, Anna Maria 5 Fiore-Donno1,3, and Rhodri Lewis1 6 7 1Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK.
    [Show full text]
  • An Ichthyophonus Hoferi Epizootic in Herring in the North Sea, the Skagerrak, the Kattegat and the Baltic Sea
    Downloaded from orbit.dtu.dk on: Oct 04, 2021 An Ichthyophonus hoferi epizootic in herring in the North Sea, the Skagerrak, the Kattegat and the Baltic Sea Mellergaard, Stig; Spanggaard, Bettina Published in: Diseases of Aquatic Organisms Link to article, DOI: 10.3354/dao028191 Publication date: 1997 Document Version Publisher's PDF, also known as Version of record Link back to DTU Orbit Citation (APA): Mellergaard, S., & Spanggaard, B. (1997). An Ichthyophonus hoferi epizootic in herring in the North Sea, the Skagerrak, the Kattegat and the Baltic Sea. Diseases of Aquatic Organisms, 28(3), 191-199. https://doi.org/10.3354/dao028191 General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. Users may download and print one copy of any publication from the public portal for the purpose of private study or research. You may not further distribute the material or use it for any profit-making activity or commercial gain You may freely distribute the URL identifying the publication in the public portal If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. DISEASES OF AQUATIC ORGANISMS Vol. 28: 191-199, 1997 Published March 27 Dis Aquat Org 1 An Ichthyophonus hoferi epizootic in herring in the North Sea, the Skagerrak, the Kattegat and the Baltic Sea 'Danish Institute of Fisheries Research, Department for Marine and Coastal Ecology.
    [Show full text]
  • Towards a Management Hierarchy (Classification) for the Catalogue of Life
    TOWARDS A MANAGEMENT HIERARCHY (CLASSIFICATION) FOR THE CATALOGUE OF LIFE Draft Discussion Document Rationale The Catalogue of Life partnership, comprising Species 2000 and ITIS (Integrated Taxonomic Information System), has the goal of achieving a comprehensive catalogue of all known species on Earth by the year 2011. The actual number of described species (after correction for synonyms) is not presently known but estimates suggest about 1.8 million species. The collaborative teams behind the Catalogue of Life need an agreed standard classification for these 1.8 million species, i.e. a working hierarchy for management purposes. This discussion document is intended to highlight some of the issues that need clarifying in order to achieve this goal beyond what we presently have. Concerning Classification Life’s diversity is classified into a hierarchy of categories. The best-known of these is the Kingdom. When Carl Linnaeus introduced his new “system of nature” in the 1750s ― Systema Naturae per Regna tria naturae, secundum Classes, Ordines, Genera, Species …) ― he recognised three kingdoms, viz Plantae, Animalia, and a third kingdom for minerals that has long since been abandoned. As is evident from the title of his work, he introduced lower-level taxonomic categories, each successively nested in the other, named Class, Order, Genus, and Species. The most useful and innovative aspect of his system (which gave rise to the scientific discipline of Systematics) was the use of the binominal, comprising genus and species, that uniquely identified each species of organism. Linnaeus’s system has proven to be robust for some 250 years. The starting point for botanical names is his Species Plantarum, published in 1753, and that for zoological names is the tenth edition of the Systema Naturae published in 1758.
    [Show full text]
  • Supplementary Material Parameter Unit Average ± Std NO3 + NO2 Nm
    Supplementary Material Table S1. Chemical and biological properties of the NRS water used in the experiment (before amendments). Parameter Unit Average ± std NO3 + NO2 nM 140 ± 13 PO4 nM 8 ± 1 DOC μM 74 ± 1 Fe nM 8.5 ± 1.8 Zn nM 8.7 ± 2.1 Cu nM 1.4 ± 0.9 Bacterial abundance Cells × 104/mL 350 ± 15 Bacterial production μg C L−1 h−1 1.41 ± 0.08 Primary production μg C L−1 h−1 0.60 ± 0.01 β-Gl nM L−1 h−1 1.42 ± 0.07 APA nM L−1 h−1 5.58 ± 0.17 AMA nM L−1·h−1 2.60 ± 0.09 Chl-a μg/L 0.28 ± 0.01 Prochlorococcus cells × 104/mL 1.49 ± 02 Synechococcus cells × 104/mL 5.14 ± 1.04 pico-eukaryot cells × 103/mL 1.58 × 0.1 Table S2. Nutrients and trace metals concentrations added from the aerosols to each mesocosm. Variable Unit Average ± std NO3 + NO2 nM 48 ± 2 PO4 nM 2.4 ± 1 DOC μM 165 ± 2 Fe nM 2.6 ± 1.5 Zn nM 6.7 ± 2.5 Cu nM 0.6 ± 0.2 Atmosphere 2019, 10, 358; doi:10.3390/atmos10070358 www.mdpi.com/journal/atmosphere Atmosphere 2019, 10, 358 2 of 6 Table S3. ANOVA test results between control, ‘UV-treated’ and ‘live-dust’ treatments at 20 h or 44 h, with significantly different values shown in bold. ANOVA df Sum Sq Mean Sq F Value p-value Chl-a 20 H 2, 6 0.03, 0.02 0.02, 0 4.52 0.0634 44 H 2, 6 0.02, 0 0.01, 0 23.13 0.002 Synechococcus Abundance 20 H 2, 7 8.23 × 107, 4.11 × 107 4.11 × 107, 4.51 × 107 0.91 0.4509 44 H 2, 7 5.31 × 108, 6.97 × 107 2.65 × 108, 1.16 × 107 22.84 0.0016 Prochlorococcus Abundance 20 H 2, 8 4.22 × 107, 2.11 × 107 2.11 × 107, 2.71 × 106 7.77 0.0216 44 H 2, 8 9.02 × 107, 1.47 × 107 4.51 × 107, 2.45 × 106 18.38 0.0028 Pico-eukaryote
    [Show full text]
  • Predatory Flagellates – the New Recently Discovered Deep Branches of the Eukaryotic Tree and Their Evolutionary and Ecological Significance
    Protistology 14 (1), 15–22 (2020) Protistology Predatory flagellates – the new recently discovered deep branches of the eukaryotic tree and their evolutionary and ecological significance Denis V. Tikhonenkov Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, 152742, Russia | Submitted March 20, 2020 | Accepted April 6, 2020 | Summary Predatory protists are poorly studied, although they are often representing important deep-branching evolutionary lineages and new eukaryotic supergroups. This short review/opinion paper is inspired by the recent discoveries of various predatory flagellates, which form sister groups of the giant eukaryotic clusters on phylogenetic trees, and illustrate an ancestral state of one or another supergroup of eukaryotes. Here we discuss their evolutionary and ecological relevance and show that the study of such protists may be essential in addressing previously puzzling evolutionary problems, such as the origin of multicellular animals, the plastid spread trajectory, origins of photosynthesis and parasitism, evolution of mitochondrial genomes. Key words: evolution of eukaryotes, heterotrophic flagellates, mitochondrial genome, origin of animals, photosynthesis, predatory protists, tree of life Predatory flagellates and diversity of eu- of the hidden diversity of protists (Moon-van der karyotes Staay et al., 2000; López-García et al., 2001; Edg- comb et al., 2002; Massana et al., 2004; Richards The well-studied multicellular animals, plants and Bass, 2005; Tarbe et al., 2011; de Vargas et al., and fungi immediately come to mind when we hear 2015). In particular, several prevailing and very abun- the term “eukaryotes”. However, these groups of dant ribogroups such as MALV, MAST, MAOP, organisms represent a minority in the real diversity MAFO (marine alveolates, stramenopiles, opistho- of evolutionary lineages of eukaryotes.
    [Show full text]
  • <I>Mucorales</I>
    Persoonia 30, 2013: 57–76 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE http://dx.doi.org/10.3767/003158513X666259 The family structure of the Mucorales: a synoptic revision based on comprehensive multigene-genealogies K. Hoffmann1,2, J. Pawłowska3, G. Walther1,2,4, M. Wrzosek3, G.S. de Hoog4, G.L. Benny5*, P.M. Kirk6*, K. Voigt1,2* Key words Abstract The Mucorales (Mucoromycotina) are one of the most ancient groups of fungi comprising ubiquitous, mostly saprotrophic organisms. The first comprehensive molecular studies 11 yr ago revealed the traditional Mucorales classification scheme, mainly based on morphology, as highly artificial. Since then only single clades have been families investigated in detail but a robust classification of the higher levels based on DNA data has not been published phylogeny yet. Therefore we provide a classification based on a phylogenetic analysis of four molecular markers including the large and the small subunit of the ribosomal DNA, the partial actin gene and the partial gene for the translation elongation factor 1-alpha. The dataset comprises 201 isolates in 103 species and represents about one half of the currently accepted species in this order. Previous family concepts are reviewed and the family structure inferred from the multilocus phylogeny is introduced and discussed. Main differences between the current classification and preceding concepts affects the existing families Lichtheimiaceae and Cunninghamellaceae, as well as the genera Backusella and Lentamyces which recently obtained the status of families along with the Rhizopodaceae comprising Rhizopus, Sporodiniella and Syzygites. Compensatory base change analyses in the Lichtheimiaceae confirmed the lower level classification of Lichtheimia and Rhizomucor while genera such as Circinella or Syncephalastrum completely lacked compensatory base changes.
    [Show full text]
  • Molecular Identity of Strains of Heterotrophic Flagellates Isolated from Surface Waters and Deep-Sea Sediments of the South Atlantic Based on SSU Rdna
    AQUATIC MICROBIAL ECOLOGY Vol. 38: 239–247, 2005 Published March 18 Aquat Microb Ecol Molecular identity of strains of heterotrophic flagellates isolated from surface waters and deep-sea sediments of the South Atlantic based on SSU rDNA Frank Scheckenbach1, Claudia Wylezich1, Markus Weitere1, Klaus Hausmann2, Hartmut Arndt1,* 1Department of General Ecology and Limnology, Zoological Institute, University of Cologne, 50923 Cologne, Germany 2Institute of Biology/Zoology, Free University of Berlin, Research Group Protozoology, 14195 Berlin, Germany ABSTRACT: Whereas much is known about the biodiversity of prokaryotes and macroorganisms in the deep sea, knowledge on the biodiversity of protists remains very limited. Molecular studies have changed our view of marine environments and have revealed an astonishing number of previously unknown eukaryotic organisms. Morphological findings have shown that at least some widely dis- tributed nanoflagellates can also be found in the deep sea. Whether these flagellates have contact with populations from other habitats is still uncertain. We performed a molecular comparison of strains isolated from deep-sea sediments (>5000 m depth) and surface waters on the basis of their small subunit ribosomal DNA (SSU rDNA). Sequences of Rhynchomonas nasuta, Amastigomonas debruynei, Ancyromonas sigmoides, Cafeteria roenbergensis and Caecitellus parvulus were analysed, and 2 contrasting results obtained. Firstly, we found nearly identical genotypes within 1 morphospecies (C. roenbergensis), and secondly, quite different genotypes within certain morpho- species (R. nasuta, A. sigmoides and C. parvulus). In addition, high genetic distances between the dif- ferent strains of A. sigmoides and C. parvulus indicate that these morphospecies should be divided into different at least genetically distinguishable species. In contrast, some heterotrophic nanoflagel- lates must indeed be regarded as being cosmopolitan.
    [Show full text]