Algal and Cyanobacteria Symbioses

Martin Grube, Joseph Seckbach, Lucia Muggia

• Publisher: WSPC (EUROPE)
• Year: 2016
• eBook ISBN: 9781786340597
• Topic: Biological Sciences
• Subtopic: Ecology
• Index: Biological Sciences

-->

Owing to their importance as primary producers of energy and nutrition, algae and cyanobacteria are found as symbiotic partners across diverse lineages of prokaryotic and eukaryotic kingdoms.

Algal and Cyanobacteria Symbioses presents a compilation of recent, updated research in fields of diverse symbioses, including in marine, freshwater, and terrestrial habitats. It gives a comprehensive overview of algal and cyanobacteria symbioses, including reviews on their diversity and information on symbiotic specificity and stress tolerance. Also covered is a review of regulatory mechanisms in the communication between symbiotic partners.

The highly interdisciplinary character of this book is demonstrated through the range of algae and cyanobacteria as energy-providing symbionts in organismal lineages which are discussed. It is a valuable source of knowledge for researchers, university lecturers, professors and students of biology and life sciences, specifically biochemistry, mycology, cell biology and plant-microbe interactions.

-->
--> Contents:

• Opening and General Aspects:
  • Symbioses Involving Photosynthetic Organisms (John A Raven)
  • Origin and Spread of Plastids by Endosymbiosis (Ugo Cenci, Daniel Moog and John M Archibald)
• Aerio-Terrestrial Symbioses:
  • Symbioses of Lichen-Forming Fungi With Trentepohlialean Algae (Martin Grube, Lucia Muggia, Elisabeth Baloch, Christina Hametner and Elfriede Stocker-Wörgötter)
  • The Lichen Photobiont Trebouxia: Towards and Appreciation of Species Diversity and Molecular Studies (Lucia Muggia, Fabio Candotto-Carniel and Martin Grube)
  • Symbiotic Cyanobacteria in Lichens (Jouko Rikkinen)
  • Symbioses of the Green Algal Genera Coccomyxa and Elliptochloris (Trebouxiophyceae, Chlorophyta) (Lydia Gustavs, Ulf Schiefelbein, Tatyana Darienko and Thomas Pröschold)
  • Investigating Mechanisms of Algal Entry into Salamander Cells (Ryan Kerney, John Burns and Eunsoo Kim)
  • Trade-Offs of Symbiotic Relationships between Aquatic Hosts and Algae in a Changing World (Daniel P Small and Cory D Bishop)
• Freshwater Symbioses:
  • Cyanobacterial Endosymbionts of Paulinella Chromatophora Shed New Light on the Birth of Cellular Organelles (Andrzej Bodył, Jakub Cieśla, Paweł Mackiewicz and Przemysław Gagat)
  • The Azolla–Anabaena –Bacteria Association: A Case of Symbiotic Abduction? (Francisco Carrapiço)
  • Symbiosis Between Green Algae and Hydra (Yoshitaka Kobayakawa)
  • Diatoms: By, with and as Endosymbionts (Patrick J Kociolek and Sarah E Hamsher)
  • Symbiosis Between Testate Amoebae and Photosynthetic Organisms (Enrique Lara and Fatma Gomaa)
• Marine Symbioses:
  • The Zooxanthellae–Hard-Coral Symbiosis (Noga Stambler)
  • Embracing Complexity in Coral–Algal Symbioses (Danielle C Claar, Nicholas S Fabina, Hollie M Putnam, Ross Cunning, Emilia Sogin, Julia K Baum and Ruth D Gates)
  • Microbial Diversity and Symbiotic Interactions with Macroalgae (Suhelen Egan, Vipra Kumar, Jadranka Nappi and Melissa Gardiner)
  • Ascophyllum and Its Symbionts — A Complex Symbiotic Community on North Atlantic Shores (David J Garbary, Norah E Brown, Hillary J MacDonell and Jantina Toxopeus)
• Stress Tolerance and Secondary Metabolism:
  • The Resistance of Lichen Photobionts to Extreme Abiotic Stressors on Earth, in Space and in Simulations (Andreas Sadowsky and Joachim Meeβen)
  • Secondary Metabolites Produced by Cyanobacteria in Symbiotic Associations (Pavel Hrouzek)
• Final Remarks:
  • Overview to Algae Symbioses (Joseph Seckbach)

-->
--> Readership: Researchers, university lecturers, professors and advanced students of biology and life sciences, specifically biochemistry, mycology, cell biology, botany, algae-specific anatomy and physiology, and plant-microbe interactions. -->

Section 1:

Aerion–Terrestrial Symbioses

Chapter 3

Symbioses of Lichen-Forming Fungi with Trentepohlialean Algae

Martin GRUBE*^,¶, Lucia MUGGIA^†,
Elisabeth BALOCH^‡, Christina HAMETNER^§
and Elfriede STOCKER-WÖRGÖTTER*

* Institute of Plant Sciences, University of Graz,
Holteigasse 6, 8010 Graz, Austria

† Università degli Studi di Trieste, Department of Life
Sciences, Via L. Giorgieri 10, 34127 Trieste, Italy

‡ Jodrell Laboratory, Royal Botanic Gardens,
Kew, Richmond, Surrey, TW9 3AB, UK

§ Department of Organismic Biology,
University of Salzburg, Hellbrunnerstraße 34,
5020 Salzburg, Austria

^¶ [email protected]

Abstract

Trentepohliaceae are a distinct lineage of green algae frequently found in association with lichen-forming fungi. We review the current knowledge about the phenotypic diversity of this group of algae, which is complemented by currently available molecular data. These data do not confirm the traditional classification of the genera based on morphological inferences. We also present more specific data on the association patterns of epiphyllous representatives in tropical rain forests. Leaf-colonizing Porina species associate specifically with Phycopeltis algae of characteristic growth types. The analysis of partial rbcL sequences of the algal partners suggests that morphologically similar growth types are genetically highly diverse and may represent different species. The fungal species may switch among morphologically similar but genetically distinct algal lineages. This strategy could promote rapid colonization of the ephemeral leaf habitats. Bark-inhabiting lichens of temperate habitats seem to represent a few known morphological species of Trentepohliales, whereas tropical bark lineages seem to be more diverse. Even though Trentepohliales are pending, a modern revision before precise figures can be given, their diversity appears to be much higher than thought before.

1.Introduction

Algae belonging to the Trentepohliaceae are often conspicuous for the bare eye by forming distinctive, yellow to orange patches in their terrestrial habitats. The pigmentation is due to the production of large amount of haematochrome (i.e., astaxanthin) at lightexposed sites. Free-living forms of these algae grow on several kinds of substrata, such as bark of trees, leaves, fruits, rocks, soils, and concrete walls. The vegetative thallus comprises filamentous colonies, which develop tiny isolated cushions or plane lawns on the substrate surfaces. Many species in free-living stage have heterotrichous thalli with prostrate and erect uniseriate filaments and exhibit various branching patterns. Some forms/genera can develop pseudoparenchymatous thalli, when the single strands are closely spaced and form compact discoid thalli. The cells are usually uninucleate and chloroplasts tend to be parietal (band-like) or reticulate (net-like) (Thompson and Wujek, 1997; López-Bautista et al., 2002).

Abundant colonies develop in habitats with high levels of humidity, such as tropical rainforests or at shaded sites in temperate regions. The order Trentepohliales is well distinguished by several characters (Rindi et al., 2009). Among them, the phragmoplast-mediated cytokinesis is unique and otherwise known only from Charophyceae and land plants (Chapman and Buchheim, 1991; Chapman et al., 2001). Within Trentepohliaceae, the classification of genera and species was based on sexual structures (Thompson and Wujek, 1997), but these are often lacking in natural samples or are not always produced in axenic conditions. The recognition of species is also complicated due to substantial morphological variation, which may be induced by ecological parameters. For these reasons, the species richness of Trentepohliaceae is still insufficiently known. Moreover, only few phylogenetic studies shed light on the higher level phylogeny and could not confirm the traditional taxonomic relationships within this group (López-Bautista and Chapman, 2003; López-Bautista et al., 2002, 2006; Rindi et al., 2009). Pioneering new molecular analyzes are available meanwhile. These studies give first insights into the patterns of selectivity in trentepohlialean lichens, but they also show that the current concept of genera is incomplete and in need of a modern revision. In this chapter, we will present an overview of the current knowledge of Trentepohlia photobiont diversity in lichens.

2.A Brief Taxonomic Account

Seventeen subaerial genera are currently classified in Trentepohliales/Trentepohliaceae: Trentepohlia Martius 1817, the largest genus in the family, Byssus Linnaeus 1753, Cephaleuros Kunze ex E.M. Fries 1832, Chrooderma F.E. Fritsch 1942, Chroolepus C. Agardh, 1824, Friedaea Schmidle 1905, Hansgirgia G.B. De Toni 1888, Lochmium Printz 1916, Mycoidea D.D. Cunningham 1879, Phycopeltis Millardet 1870, Physolinum Printz 1921, Printzina R.H. Thompson and D.E. Wujek 1992, Rhizothallus P. Dangeard 1931, Spongioplastidium Vischer 1933, Sporocladus Kuckuck 1897, Stomatochroon B.T. Palm 1934 and Tophora E.M. Fries 1825 (Guiry and Guiry, 2014). Species of the genera Trentepohlia and Printzina are very common epiphytes but also occur on plastic, rock, and masonry. The genus Byssus comprises 25 species, at which only species are currently accepted taxonomically whereas the remaining ones are considered as synonyms for diverse algae of the genera Aphanizomenon A. Morren ex Bornet and Flahault 1888, Cladophora Kützing 1843, Hydrodictyon Roth 1797, Rhodochorton Nägeli 1862, Trentepohlia and Vaucheria A.P. de Candolle 1801. The type species of Byssus constitutes Trentepohlia jolithus (Linnaeus) Wallroth 1833 (Guiry and Guiry, 2014). Cephaleuros is known as obligate endophyte which grows below the cuticle or extends into the mesophyll of host plants. Cephaleuros endophyticus (F.E. Fritsch) Printz 1964 represents the type species of the genus Chrooderma that includes C. endophytica F.E. Fritsch 1942 as single species. In the case of the genus Chroolepus it is just to mention that all 43 species provide as synonyms for different algal species of the genus Trentepohlia, some of Printzina lagenifera (Hildebrand) R.H. Thompson and D.E. Wujek 1992, Chroolepus amboinensis Karsten 1891 is renamed as Phycopeltis amboinensis (Karsten) Printz 1939, and three Chroolepus-species are of unknown origin. Algae of the genus Friedaea are found in moving water in Europe and form hemispherical, lime-encrusted tufts composed of uniseriate, pale green branched filaments (Schmidle, 1905). The genus Hansgirgia comprises three species which are synonymous with Phycopeltis flabelligera De Toni 1888, P. irregularis (Schmidle) Wille 1909 and P. prostrata (De Wildeman) Schmidle 1897. Lochmium piluliferum Printz 1918 is the only known species of this genus. The thallus structure has similar branching patterns as algae of the genus Microthamnion Nägeli 1849, but the cells of Lochmium piluliferum are broader, club-shaped or ovoid, have thicker cell walls, and produce terminal akinetes. This alga was collected from brackish-water in Siberia (Guiry and Guiry, 2014). Only one algal species, Mycoidea parasiticus Cunningham 1879, represents the genus Mycoidea which is taxonomically accepted under the name Cephaleuros virescens Kunze ex E.M. Fries 1832 yet. Phycopeltis develops primarily on smooth surfaces such as vascular stem and leaf tissue, but also on artificial material such as plastic, metal, etc. (Rindi and Guiry, 2002). Algae of the genus Physolinum can be found under the species name Trentepohlia rigidula (J. Müller) Hariot 1889 which form compact crusts on tree bark, especially at weather-exposed sites. The thallus consists of entangled filaments in which sometimes prostrate and erect systems are developed and vary in color becoming dark red, pink, orange or yellow (Rindi et al., 2008). The next three genera comprise each only a single algal species respectively, e.g., Rhizothallus islandicus P. Dangeard 1931 (collected in Iceland), Spongioplastidium proliferum Vischer 1933 (collected in Switzerland), and Sporocladus fragilis Kuckuck 1897 (collected in Helgoland). Stomatochroon is an obligate endophyte and develops beneath the stomata of plants. The filaments grow also into the stomatal chamber and produce additional plantlets at other stomata (Palm, 1934). The last genus Tophora comprises only the species T. cryptarum E.M. Fries which indeed represents a synonym for Trentepohlia aurea (Linnaeus) C.F.P. Martius 1817.

Apart from forming free-living colonies, trentepohlialean algae are frequently found to be involved in biotic interactions. One of the genera, Cephaleuros, includes several species known as pathogens of higher plants, but most of the interactions are mutualistic lichen symbioses with fungi.

3.Lichenized Fungal Lineages with Trentepohlialean Photobionts

Approximately one-fifth of lichen-forming fungi are involved in symbiosis with algae of the family Trentepohliaceae worldwide. The mapping of associated algal groups on the phylogeny of the species’ richest group of lichenized fungi (Lecanoromycetes) reveals large scale patterns of lichen partnerships (Miadlikowska et al., 2004, 2014). The majority of mycobiont species constituting the larger lineages preferentially associates with likewise big phyletic lineages of photobionts, either cyanobacteria, coccal or filamentous green algae (Trentepohliaceae). Despite this general trend of association, switches to other photobiont types are observed within some lineages (e.g., between groups of eukaryotic algae in Arthoniomycetes). Few instances suggest that switches may occur between closely related species, and this also includes lineages which normally associate with algae of Trentepohliales (e.g., Petractis clausa associating with Trentepohlia and P. hypoleuca with cyanobacteria). On the other hand, phycosymbiodemes (independent thalli formed by the same mycobiont with different photobiont types) have not been observed in any of the Trentepohlia lichen symbioses.

Ecological parameters seem to influence a general pattern of association of fungi with different groups in Trentepohliaceae. For example, lichens on bark or rock usually associate with algae assigned to the genus Trentepohlia, whereas epiphyllous lichens frequently associate with Cephaleuros and Phycopeltis (a genus characterized by two-dimensional colonies). Patterns at a more detailed level were hardly ever investigated, due to the difficulties in determining the trentepohlialean photobiont species.

4.Interfacing with Fungi

Interactions of lichen mycobionts with Trentepohliaceae have so far been studied only by microscopic methods. In most bark- and rock-inhabiting lichens, the filaments normally observed in free-living trentepohlialean algae appear fragmented to threads of few cells in length in the lichenized stage. Morphological patterns are therefore poorly developed in comparison with free-living strains. These algae are then arranged in a more or less distinct algal layer in the thallus structure; if this layer is well developed it is usually bordered apically by a cortex and basally by medulla or another structure made of the fungal partner. This fungal dominance is less distinct in most lichens growing on living leaves (epiphyllous lichens) and in a few lichens developing on bark or rock (such as Coenogonium). In epiphyllous lichens, typicall...

Table of contents

• Cover Page
• Title
• Copyright
• Contents
• Foreword
• Acknowledgments
• About the Editors
• List of Contributors
• Opening and General Aspects
• Section 1: Aerion–Terrestrial Symbioses
• Section 2: Freshwater Symbioses
• Section 3: Marine Symbioses
• Section 4: Stress Tolerance and Secondary Metabolism
• Final Remarks
• Index