Tai Lieu Chat Luong ALGAE A N ATO M Y, B I O C H E M I S T RY, A N D B I OT E C H N O LO G Y SECOND EDITION ALGAE A N ATO M Y, B I O C H E M I S T RY, A N D B I OT E C H N O LO G Y SECOND EDITION L AURA BARSANTI • PAOLO GUALTIERI Istituto di Biofisica Pisa, Italy CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 © 2014 by Taylor & Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group, an Informa business No claim to original U.S Government works Version Date: 20130827 International Standard Book Number-13: 978-1-4398-6733-4 (eBook - PDF) This book contains information obtained from authentic and highly regarded sources Reasonable efforts have been made to publish reliable data and information, but the author and publisher cannot assume responsibility for the validity of all materials or the consequences of their use The authors and publishers have attempted to trace the copyright holders of all material reproduced in this 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the CCC, a separate system of payment has been arranged Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com and the CRC Press Web site at http://www.crcpress.com Alla Lilli, perché è sempre la mia mamma, anche se mi fa diventare matto come quando ero piccino [(ti voglio bene, mamma!)] Paolo To my mom, Silvana (1926–2008), and my dad, Renzo (1928–2009), because I know they are still watching over me, and to Bernard (1952–2011) pour son voyage en solitaire (nakupenda tarepanda) Laura Contents Preface xiii Authors xv Chapter General Overview Definition .1 Classification Occurrence and Distribution Structure of Thallus—Cytomorphological Types .6 Unicells and Unicell Colonial Type .8 Filamentous Type 10 Siphonocladous Type 13 Siphonous Type 13 Parenchymatous and Pseudo-Parenchymatous Type 14 Palmelloid Type 15 Nutrition 16 Reproduction 17 Vegetative and Asexual Reproduction 17 Binary Fission or Cellular Bisection 17 Zoospore, Aplanospore, and Autospore 18 Autocolony Formation 18 Fragmentation 18 Resting Stages 18 Sexual Reproduction .20 Haplontic or Zygotic Life Cycle .20 Diplontic or Gametic Life Cycle 20 Diplohaplontic or Sporic Life Cycles 20 Summaries of the 11 Algal Phyla 22 Cyanobacteria 22 Glaucophyta 24 Rhodophyta 25 Chlorophyta 29 Charophyta 32 Haptophyta 33 Cryptophyta 35 Ochrophyta 35 Cercozoa—Chlorarachniophyceae 39 Myzozoa—Dinophyceae 39 Euglenozoa—Euglenophyceae 41 Endosymbiosis and Origin of Eukaryotic Photosynthesis 42 Suggested Reading 46 Chapter Anatomy 49 Cytomorphology and Ultrastructure 49 Outside the Cell 49 vii viii Contents Type 1—Simple Cell Membrane 49 Type 2—Cell Surface with Additional Extracellular Material 50 Type 3—Cell Surface with Additional Intracellular Material in Vesicles 60 Type 4—Cell Surface with Additional Extracellular and Intracellular Material 62 Flagella and Associated Structures 66 Flagellar Shape and Surface Features 68 Flagellar Scales 68 Flagellar Hairs 70 Flagellar Spines 72 Internal Features of the Flagellum 72 Axoneme 72 Paraxial Rod 73 Other Intraflagellar Accessory Structures 74 Transition Zone 75 Basal Bodies 79 Root System 82 How Algae Move 93 Swimming 93 Movements Other than Swimming 99 Buoyancy Control 100 How a Flagellum Is Built: The Intraflagellar Transport 102 How a Flagellar Motor Works 103 How a Paraxial Rod Works 104 The Photoreceptor Apparata 104 Types of Photoreceptive Systems 106 Type I 106 Type II 108 Type III 109 Photoreceptive Proteins 111 Fundamental Behavioral and Physiological Features 111 Sampling Strategies 112 Trajectory Control 113 Signal Transmission 114 An Example: Photoreceptor and Photoreception in Euglena 114 Chloroplasts 118 The Nucleus, Nuclear Division, and Cytokinesis 126 Ejectile Organelles and Feeding Apparata 132 Suggested Reading 137 Chapter Photosynthesis 141 Light 141 Photosynthesis 144 Light-Dependent Reactions 145 PSII and PSI: Structure, Function, and Organization 153 ATP Synthase 155 ETC Components 155 Electron Transport: The Z-Scheme 157 Proton Transport: Mechanism of Photosynthetic Phosphorylation 158 Contents ix Pigment Distribution in PSII and PSI Super-Complexes of Algal Division 160 Light-Independent Reactions 160 RuBisCO 166 Calvin–Benson–Bassham Cycle 167 Carboxylation 167 Reduction 167 Regeneration 167 Photorespiration 168 The Energy Relationships in Photosynthesis: The Balance Sheet 168 Suggested Reading 170 Chapter Working with Light 173 How Light Behaves 173 Scattering 173 Absorption 174 Interference 175 Reflection 175 Refraction 177 Dispersion 178 Diffraction 178 Field Instruments: Use and Application 181 Radiometry 181 Measurement Geometries: Solid Angles 181 Radiant Energy 182 Spectral Radiant Energy 182 Radiant Flux (Radiant Power) 182 Spectral Radiant Flux (Spectral Radiant Power) 182 Radiant Flux Density (Irradiance and Radiant Exitance) 182 Spectral Radiant Flux Density 183 Radiance 183 Spectral Radiance 184 Radiant Intensity 184 Spectral Radiant Intensity 185 Photometry 185 Luminous Flux (Luminous Power) 185 Luminous Intensity 185 Luminous Energy 188 Luminous Flux Density (Illuminance and Luminous Exitance) 188 Luminance 188 Lambertian Surfaces 188 Units Conversion 189 Radiant and Luminous Flux (Radiant and Luminous Power) 189 Irradiance (Flux Density) 190 Radiance 190 Radiant Intensity 190 Luminous Intensity 190 Luminance 190 Geometries 190 PAR Detectors 191 The Photosynthesis–Irradiance Response Curve (P vs E Curve) 193 Oddities and Curiosities in the Algal World 313 Motile stages and their accompanying basal bodies and flagellar roots have never been observed These algae lack the green light-harvesting photosynthetic pigments siphonoxanthin and siphonein typically found in other low-light adapted green algae, but adapt to low-light conditions by maintaining high concentration of chlorophyll b, which absorbs the blue-green light of deeper water more efficiently than chlorophyll a The interest in the Palmophyllales is strictly connected to their deep-branching position, which raises questions about the nature of the green plant ancestor, generally accepted to be a unicellular flagellate The molecular phylogenetic evidence that the nonflagellate Palmophyllales form a distinct and early diverging lineage of green algae indicates that the green plant ancestor could have been a nonmotile unicellular organism, maybe possessing transient motile stages A separate mention has to be reserved for other benthic primary producers, thriving at very dimly lit deep-water habitats, that is, corals, invertebrates in intimate endosymbiosis with photosynthetic dinoflagellates of the genus Symbiodinium (zooxanthellae) The deepest known hermatypic coral reefs are mainly located in Jamaica and Bahamas, at a depth of around 70 m Recently, a deepwater coral community has been discovered at Pulley Ridge off the southwest coast of Florida, in waters 58–75 m deep At these depths, large areas with up to 60% live coral coverage are present; the zooxanthellate scleractinian coral Agaricia sp is one of the most abundant hermatypic corals in southern Pulley Ridge, forming tan-brown plates up to 50 cm in diameter The corals generally appear to be healthy, with no obvious evidence of coral bleaching or disease, though they appear to be thriving on 1–2% (5–30 µmol m−2 s−1) of the available surface light (PAR) and about 5% of the light typically available to shallow-water reefs (500–1000 µmol m−2 s−1) Besides zooxanthellate corals, the deepest portion of the photic zone also hosts antiphatarians, commonly known as black corals These organisms have traditionally been considered an exclusive azooxanthellate order of anthozoan hexacorals, a trait thought to reflect their preference for lowlight environments that not support photosynthesis They occur in dimly lit to dark areas in both shallow water, where they are present in shaded microenvironments, and deep water, where they are effectively shaded by light intensities decreasing with depth ITS2 genotyping and histology performed on antiphatarian species collected from the Hawaian Islands and Johnston Atoll at depths between 10 and 396 m detected Symbiodinium cells in all the samples collected down to below the compensation depth for photosynthesis in Hawaian waters (approx 125 m) This study represents the deepest record for Symbiodinium, indicating that at least some members of this dinoflagellate genus have incredibly diverse habitat preferences and broad environmental ranges Moreover, these findings suggest that the carbon demand of these dinoflagellate is either reduced by dormancy or met by means other than photosynthesis, such as by self-digestion or by heterothrophic feeding on an external carbon source Heterotrophic endosymbiont feeding has been suggested in zooxanthellate invertebrates that are seasonally exposed to environmental conditions that not support photosynthesis, and these modes of nutrition would make sense for Symbiodinium populations located below the compensation depth for photosynthesis Low-light habitats are not limited to aquatic environments, but they are present also in subaerial locations, such as hypogea The most comprehensive studies of subaerial biofilms have been carried out on the three catacomb sites dedicated to St Domitilla, St Callistus, and Priscilla in Rome, Italy, and on Maltese paleo-Christian catacombs situated in Rabat and Paola Micro-environmental parameters (light intensity/photoperiod, degree of wetness of the surface, relative humidity, temperature) determine which microorganisms prevail in a specific hypogeum, but the undisputed phototrophic protagonists in subaerial biofilms are filamentous cyanobacteria Different species of terrestrial epilithic cyanobacteria belonging to the genera Eucapsis Clements et Shantz 1909, Leptolyngbya Anagnostidis et Komárek 1988, Scytonema Agardh ex Bornet et Flahault 1887, and Fischerella lahault Gomont 1895 occur as dominant organisms in these phototrophic microbial communities Some of these taxa have never been recorded outside of these habitats and for this reason are defined as “troglobitic,” that is, obligate cavernicole taxa unable to survive outside of caves 314 Algae or other low-light environments Subaerophytic troglobitic cyanobacteria belonging to the genus Leptolyngbya are particularly abundant in phototrophic biofilms present in both Roman and Maltese hypogea These cyanobacteria live under extremely low photon fluxes, rarely exceeding 10 µmol m−2 s−1, similar to deep-water algae At this extremely low photon fluxes, these algae can grow because of the presence of phycobiliproteins organized in phycobilisomes in the thylakoid membranes inside the cell that transfer their absorbed extra energy to chlorophylls They sense the light direction by means of a photoreceptive apparatus that is located in the apical portion of the tip cell, which is composed by a carotenoid-containing screening device and a light detector based on rhodopsin-like proteins (refer to Chapter 2) ALGAE–ANIMAL INTERACTION: RIDING A SLOTH, SWINGING ON A SPIDER WEB, SWIMMING IN A JELLY Algae are involved into complex relationships with very different animals They have been reported to grow epizoic on sloths, polar bears, seals, frogs and salamanders, arthropods, and turtles In the following, we will describe the most unusual associations between these quite distant biological groups A very particular symbiosis is that between sloths and green algae Sloths are slow-moving arborean mammals inhabiting tropical rainforest in Central and South America, represented by two genera, Bradypus, the three-toed sloths, and Chaelopus, the two-toed sloths A versatile small-scale ecosystem that includes algae, ciliates, and fungi thrives in the sloth fur The greenish color of the hair, especially evident in Bradypus species, is due to green algae belonging to the algal classes Ulvophyceae and Trebouxiophyceae These algae effectively turn these animals green, giving them excellent camouflage among the leaves The camouflage is crucial to the sloth’s survival, because its inability to move quickly makes it an easy target for predators such as the harpy eagle (Harpia harpyja) Among the many odd features of these interesting animals, perhaps the oddest of all is their hair which, with its peculiar structure and its algal presence, is unlike the hair of any other mammal Sloth hair is long and coarse and that of the two living species belonging to the genus Chaelopus is unique in having a number of deep groves running the length of each hair, whereas the hair of the four species belonging to genus Bradypus has irregular transverse cracks that increase in number and size with age During the dry season, the hair of sloths usually has a dirty brown coloration, but during a long period of rain it may show very appreciable greenish tinges brought about by the increased presence of symbiotic algae Recently, the genetic diversity of the eukaryotic community present in the fur of sloths belonging to all six extant species was investigated The majority of the green algal sequences obtained from the hair samples formed a clade of their own within the green algal class Ulvophyceae (Chlorophyta) This group received high support (100%) for its monophyly in all phylogenetic analyses that were employed This clade, consisting of small (3–13 μm) thick-walled cells without pyrenoids, is likely to correspond to the green algal genus Trichophilus, whose first description dates back to 1887 The clade was subdivided into three subclades that received moderate-to-high internal node support Two subclades, A and C, were formed by rRNA gene clones originating from Choloepus hoffmanni hair samples Clones in the clade B originated from the hair of Bradypus species Within clade B, the sequences from Bradypus tridactylus were different from those of B variegatus and B pygmaeus Trichophilus spp was the only green alga in the hair of the brown-throated sloth B variegatus and the pygmy three-toed sloth B pygmaeus These species were also found on Hoffmann’s twotoed sloth C hoffmanni and the pale-throated sloth B tridactylus, together with terrestrial green algae from their surroundings, such as Trentepohlia (Ulvophyceae, Chlorophyta) and Myrmecia (Trebouxiophyceae, Chlorophyta), while the maned three-toed sloth B torquatus hosted a variety of purely terrestrial algae The algae have a distinct distribution patterns in Choloepus and Bradypus, lying longitudinally along the grooves in the former and in short lateral tongue or lines in the latter The algae found on the Oddities and Curiosities in the Algal World 315 coat of B tridactylus lie between the cuticle scales and the hair changes with age in apparently all species of Bradypus Young hairs are white, gray, brownish, or black and not possess the deep cracks seen in older hairs The first traces of algae appear on these young hairs as tiny dots or extremely narrow transverse lines Older hairs have larger, wider algal colonies and obvious deep transverse cracks When wet, these cracks close considerably, but when dry give the effects of beads on a string The oldest hairs are badly deteriorated with the spongy cuticle worn off on one side exposing the full length of the cortex In the older hairs, living algae are absent It was suggested that either the algae colonize the very narrow cracks in young hairs or the algae themselves initiate the cracks The hair of all the three Bradypus species readily absorbs water, but those of Choloepus not No evidence of algae were found in babies still at the age of clinging to their mothers, suggesting that at least Trichophilus is gained in childhood, most likely from the mother This observation is supported by an earlier study noting that sloths gain the algae and other parasites by the time they are a few weeks old, which could provide them a protective camouflage Lack of healthy algal colonies has been observed in Bradypus kept in captivity; since they not survive long under these conditions, algae have been suggested to provide nutrition or a particular trace element essential for the health of the animals Algae have reported to grow also on the fur of polar bears (Thalarctos maritimus) These animals normally have creamy-white fur, presumably an adaptation for camouflage in a snowy environment However, cases are being reported of polar bears kept in captivity in different American and Japanese zoos, which turned green as a result of algae growing on their fur The coloration was particularly evident on the flanks, on the outer fur of the legs, and in a band across the rump This coloration was clearly attributable to the presence of algae inside the hairs, specifically in the hollow medullae of many of the wider (50–200 µm), stiffer guard hairs of the outer coat The thinner (30 m) macroalgae in central California Journal of Phycology, 39(2), 273–284, 2003 Spijkerman E., A Wacker, G Weithoff, and T Leya Elemental and fatty acid composition of snow algae in arctic habitats Frontiers in Microbiology, 3, 2012 Su Y., X Zhao, A Li, and X Li, G Huang Nitrogen fixation in biological soil crusts from the Tengger Desert, northern China European Journal of Soil Biology, 47(3), 182–187, 2011 Suutari M., M Majaneva, D Fewer, B Voirin, A Aiello, T Friedl et al Molecular evidence for a diverse green algal community growing in the hair of sloths and a specific association with Trichophilus welckeri (Chlorophyta, Ulvophyceae) BMC Evolutionary Biology, 10(1), 86, 2010 Tattersall, G.J and N Spiegelaar Embryonic motility and hatching success of Ambyostoma maculatum are influenced by a symbiotic algae Canadian Journal of Zoology, 86, 1289–1298, 2008 Tumlison R and S.E Trauth A novel facultative mutualistic relationship between bufonid tadpoles and flagellated green algae Herpetological Conservation and Biology, 1(1), 51–55, 2006 Wagner, D., X Pochon, L Irwin, R.J Toonen, and R.D Gates Azooxanthellate? Most Hawaiian black coral contain Symbiodinium Proceedings of Royal Society B, 278, 1323–1328, 2011 Wang G., K Chen, L Chen, C Hu, D Zhang, and Y Liu The involvement of the antioxidant system in protection of desert cyanobacterium Nostoc sp against UV-B radiation and the effects of exogenous antioxidants Ecotoxicology and Environmental Safety, 69(1), 150–157, 2008 Ward D.M., M.M Bateson, M.J Ferris, M Kühl, A Wieland, A Koeppel et al Cyanobacterial ecotypes in the microbial mat community of Mushroom Spring (Yellowstone National Park, Wyoming) as species-like units linking microbial community composition, structure and function Philosophical Transactions of the Royal Society B: Biological Sciences, 361(1475), 1997–2008, 2006 Yan-Gui S., L Xin-Rong, C Ying-Wu, Z Zhi-Shan, and L Yan Carbon fixation of cyanobacterial–algal crusts after desert fixation and its implication to soil organic carbon accumulation in desert Land Degradation & Development, 24(4), 342–349, 2013 Zammit G., D Billi, E Shubert, J Kaštovsk, and P Albertano The biodiversity of subaerophytic phototrophic biofilms from Maltese hypogea Fottea, 11(1), 187–201, 2011 Zhao J., B Zhang, and Y Zhang Chlorophytes of biological soil crusts in Gurbantunggut Desert, Xinjiang Autonomous Region, China Frontiers of Biology in China, 3(1), 40–44, 2008 Biological Sciences “ stands out for its in-depth information on structural and mechanical anatomy, with flagella as the most prominent example The meticulous and elegant drawings of algal apparatuses and their mechanics make it easy to understand complex structures and functions, as well as constitutes another outstanding feature of this book.” —Senjie Lin, Marine Sciences, University of Connecticut, Groton, The Quarterly Review of Biology, Vol 81, December 2006 “ the authors concentrate on highlighting interesting and illuminating topics, with the idea of inciting the sort of wonder and curiosity that will encourage further outstanding research.” —Willem F Prud’homme van Reine, Blumea, 2006, Vol 51, No.3 A single-source reference on the biology of algae, Algae: Anatomy, Biochemistry, and Biotechnology, Second Edition examines the most important taxa and structures for freshwater, marine, and terrestrial forms of algae Its comprehensive coverage goes from algae’s historical role through its taxonomy and ecology to its natural product possibilities The authors have gathered a significant amount of new material since the publication of the first edition This completely revised second edition contains many changes and additions including the following: • • • • • • All revised and rewritten tables, plus new figures, many in color A fascinating new chapter: Oddities and Curiosities in the Algal World Expanded information on algal anatomy Absorption spectra from all algal divisions, chlorophylls, and accessory pigments Additional information on collection, storage, and preservation of algae Updated section on algal toxins and algal bioactive molecules The book’s unifying theme is on the important role of algae in the earth’s self-regulating life support system and its function within restorative models of planetary health It also discusses algae’s biotechnological applications, including potential nutritional and pharmaceutical products Written for students as well as researchers, teachers, and professionals in the field of phycology and applied phycology, this new full-color edition is both illuminating and inspiring K13023