Marine Algae: Biodiversity, Taxonomy, Environmental Assessment, and Biotechnology

Marine Algae

Biodiversity, Taxonomy, Environmental

Assessment, and Biotechnology

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Marine Algae

Biodiversity, Taxonomy, Environmental

Assessment, and Biotechnology

Editors

Leonel Pereira and João M. Neto

Department of Life Sciences

IMAR-CMA and MARE

(Marine and Environmental Sciences Centre)

University of Coimbra

Coimbra

Portugal

A SCIENCE PUBLISHERS BOOK

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GL--Prelims with new title page.indd ii 4/25/2012 9:52:40 AM

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Preface

This is a book consisting of 11 chapters covering three thematic areas of

great impact in modern societies. Based on the main web site of algae

(www.algaebase.org), developed in Chapter 11, it includes a revision of the

taxonomy used on algae studies, as well as general aspects of biology and the

methodologies used in this sector of marine biology (Chapter 1). The second

thematic area comprises fi ve chapters (Chapter 2 to Chapter 5) focused on

the use of algae as potential environmental sentinels; the threats that algae

may represent when dispersed around the world due to the uncontrolled

commercial trades’ activity; and their use for a sustainable modern world.

Following the conservational concerns presently implemented in most

Western economies and some emerging countries, this information is of

vital importance for a proper management of aquatic environments, and

the sustainable management of their natural resources. The third area is

centered on the use of different strands of algae and its potential use in the

industrial sector: food (human and animal feed), pharmaceutical, cosmetics,

and agricultural fertilizers (Chapter 6 to Chapter 10).

This book is intended to fi nd a wide market of potential users, from the

academic fi eld, research institutions and industry, to government agencies

responsible for the implementation of integrated management of natural

resources and environmental quality assessment of aquatic systems. Two

added values of the book are: i) the wide experience the authors of different

chapters possess in different marine biology research areas; and ii) the

combination of the potential uses of algae in modern society (industry) with

a sustainable use of natural resources of aquatic ecosystems.

A special acknowledgement is addressed to our colleague Dr. Joana

Patrício by her great contribution and productive discussions had initially

to structure and select the contents of the book.

Leonel Pereira

João M. Neto

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Contents

Preface v

1. Marine Algae: General Aspects (Biology, Systematics, 1

Field and Laboratory Techniques)

Tomás Gallardo

2. Searching for Ecological Reference Conditions of Marine 68

Macroalgae

Rui Gaspar, João M. Neto and Leonel Pereira

3. Marine Macroalgae and the Assessment of Ecological 97

Conditions

João M. Neto, José A. Juanes, Are Pedersen and Clare Scanlan

4. Understanding Biological Invasions by Seaweeds 140

Fátima Vaz-Pinto, Ivan F. Rodil, Frédéric Mineur, Celia Olabarria

and Francisco Arenas

5. Marine Algae as Carbon Sinks and Allies to Combat 178

Global Warming

Francisco Arenas and Fátima Vaz-Pinto

6. Review of Marine Algae as Source of Bioactive Metabolites: 195

a Marine Biotechnology Approach

Loïc G. Carvalho and Leonel Pereira

7. Analysis by Vibrational Spectroscopy of Seaweed with 228

Potential Use in Food, Pharmaceutical and Cosmetic

Industries

Leonel Pereira and Paulo J.A. Ribeiro-Claro

8. Kappaphycus (Rhodophyta) Cultivation: Problems and the 251

Impacts of Acadian Marine Plant Extract Powder

Anicia Q. Hurtado, Renata Perpetuo Reis, Rafael R. Loureiro and

Alan T. Critchley

viii Marine Algae

9. Marine Algae and the Global Food Industry 300

Maria Helena Abreu, Rui Pereira and Jean-François Sassi

10. Marine Macroalgae and Human Health 320

Sarah Hotchkiss and Catherine Murphy

11. Internet Information Resources for Marine Algae 357

Michael D. Guiry and Liam Morrison

Index 377

Color Plate Section 381

CHAPTER 1 HAPTER 1

Marine Algae: General Aspects (Biology,

Systematics, Field and Laboratory

Techniques)

Tomás Gallardo

1 Introduction

Today, algae are not a taxonomic category. However, the term is very useful

for grouping both prokaryotic organisms, in which cell organelles are not

delimited by membranes, and eukaryotic organisms, in which they are.

Considering biochemical criteria, their ecological affi nities and common

photosynthesis with oxygen production, in this chapter we will focus on

both photosynthetic bacteria with chlorophyll a, division Cyanophyta, and

the different divisions of eukaryotic algae.

Algae are simple organisms. Many are unicellular, while others are

multicellular and more complex, but they all have rudimentary conducting

tissues. They also exhibit a wide range of variation from a morphological

and reproductive point of view. Algae are biochemically and physiologically

very similar to the rest of plants: they essentially have the same metabolic

pathways, possess chlorophyll, and produce similar proteins and

carbohydrates. Some algae, such as euglenophytes, dinophytes and

ochrophytes, have lost their photosynthetic capacity and live as saprophytes

or parasites. However, there are also representatives of other groups, such

as green algae, in which more than a hundred heterotrophic species have

been described. An essential characteristic which distinguishes algae from

other photosynthetic plants is their lack of an embryo and multicellular

Dep. Biología Vegetal, Universidad Complutense, 28040 Madrid, Spain.

Email: [email protected]

2 Marine Algae

envelope around the sporangia and gametangia (except for freshwater

green algae, charophytes). Algae are different from fungi in that they lack

photosynthetic capacity.

Algae have been estimated to include anywhere from 30,000 to more

than one million species, most of which are marine algae (Guiry 2012). The

most accurate estimate obtained from Algabase (Guiry and Guiry 2013) cites

over 70,000 species, of which about 44,000 have probably been published.

It is still not well known how many species comprise some groups. For

diatoms, some phycologists estimate a number of over 200,000 species.

Algae are ubiquitous and live in virtually all media. Although they are

mainly related to aquatic habitats, they can also develop on the ground

or on snow and ice, as these living organisms tolerate the most extreme

temperatures. In aquatic ecosystems, they are the most important primary

producers, the base of the food chain.

The classifi cation of algae has experienced great changes over the

last thirty years, and today there is no general scheme accepted by all

phycologists. There are several systematic proposals, ranging between 5

and 16 divisions. Different treatments are found in Bold and Wynne (1978),

South and Whittick (1987), Dawes (1998), Margulis et al. (1989), Hoek et

al. (1995), Johri et al. (2004), Barsanti and Gualtieri (2006), Lee (2008) and

Graham et al. (2009). In this text, the adopted system is summarized in

Table 1. It partly follows the recommendations of Yoon et al. (2006) for red

algae, those of Leliaert et al. (2012) for green algae, and those of Riisberg et

al. (2009) and Yoon et al. (2009) for ochrophytes, as well as data compiled

by Algabase (Guiry and Guiry 2013).

2 General Aspects

Algae are unicellular or multicellular organisms which, with the exception

of the cyanophytes, have cellular organelles surrounded by membranes. All

autotrophic algae have chlorophyll a and the accessory pigment β-carotene.

Sexual reproduction by means of specialized cells involves alternating

nuclear phases and a zygote that never develops a multicellular embryo. In

general, the cells of eukaryotic algae are surrounded by a wall produced by

the Golgi apparatus. The wall in most of them has a fi brillate appearance,

because it consists of cellulose, often containing polysaccharides formed

by amorphous mucilage. Their cells have numerous organelles, among

which the mitochondria, chloroplasts and nucleus are the only organelles

surrounded by a double membrane (Fig. 1a). Invaginations of the inner

membrane of mitochondria, called mitochondrial crests, can have two

different shapes. They are laminar in algae with phycobiliproteins and in

those with both chlorophyll a and b (Table 2), whereas they are tubular in

the rest of the groups (Roy et al. 2011).

Marine Algae: General Aspects 3

Table 1. Classifi cation scheme of different algal groups.

Kingdom Phylum Subphylum Class

Prokaryota

eubacteria

Cyanophyta Cyanophyceae

Eukaryota Glaucophyta Glaucophyceae

Rhodophyta Cyanidiophytina Cyanidiophyceae

Eurhodophytina Compsopogonophyceae

Porphyridophyceae

Rhodellophyceae

Stylonematophyceae

Bangiophyceae

Florideophyceae

Cryptophyta Cryptophyceae

Dinophyta Dinophyceae

Haptophyta Haptophyceae

Ochrophyta Khakista Bacillariophyceae

Bolidophyceae

Phaeista Chrysophyceae

Synurophyceae

Eustigmatophyceae

Raphidophyceae

Dictyochophyceae

Pelagophyceae

Pinguiophyceae

Phaeothamniophyceae

Chrysomerophyceae

Xanthophyceae

Phaeophyceae

Euglenophyta Euglenophyceae

Chlorarachniophyta Chlorarachniphyceae

Chlorophyta Prasinophytina Prasinophyceae

Tetraphytina Chlorophyceae

Chlorodendrophyceae

Trebouxyophyceae

Ulvophyceae

Dasycladophyceae

Charophyta

(Streptophyta p. p.)

Coleochaetophyceae

Conjugatophyceae

Mesotigmatophyceae

Klebsormidiophyceae

Charophyceae

4 Marine Algae

Figure 1. Ultrastructure of the fl agellate male gamete of a central diatom. (a) Longitudinal

section through whole cell. (b) Cross section through the fl agellum; note the absence of the

central pairs of the microtubules. (c) Detail of the chloroplasts with girdle lamella. B: base

of mastigoneme. CE: chloroplast envelope. CER: chloroplast endoplasmic reticulum. CH:

chloroplast. CN: chloroplasts nucleoid. GL: girdle lamella. L: lamella composed of a stack of

three thylacoids. M: mitochondrion. N: nucleus. NE: nuclear envelope. PM: plasma membrane.

S: tubular part of mastigoneme. TF: terminal fi ber of mastigoneme (After Hoek et al. 1995).

Marine Algae: General Aspects 5

Table 2. The main pigments of the algal phyla.

Phylum Chlorophylls Phycobilins Carotenoids Xanthophylls

Cyanophyta a and a, b Allophycocyanin β-Carotene Myxoxanthin

c-Phycoerythrin Zeaxanthin

c-Phycocyanin

Glaucophyta a Allophycocyanin β-Carotene Zeaxanthin

c-Phycocyanin

Rhodophyta a, d Allophycocyanin α-, β-Carotene Lutein

r-Phycoerythrin

r-Phycocyanin

Cryptophyta a, c Phycoerythrin α-, β-,

ε-Carotene

Alloxanthin

r-Phycocyanin

Dinophyta a, b, c Absent β-Carotene Diadinoxanthin

Peridinin

Fucoxanthin

Dinoxanthin

Haptophyta a, c Absent α-, β-Carotene Fucoxanthin

Ochrophyta a, c1

, c2

, c3 Absent α-, β-,

ε-Carotene

Fucoxanthin

Violaxanthin

Diadinoxanthin

Heteroxanthin

Vaucheriaxanthin

Euglenophyta a, b Absent β-, γ-Carotene Diadinoxanthin

Chlorarachniophyta a, b Absent β-Carotene/

absent

Lutein

Violaxanthin

Neoxanthin

Siphonaxanthin

Chlorophyta a, b Absent α-, β-,

γ-Carotene

Lutein

Prasinoxanthin

Charophyta

(Streptophyta p.p.)

a, b Absent α-, β-,

γ-Carotene

Lutein

The pigments responsible for photosynthesis are located in a membrane

system in the form of fl at vesicles called thylakoids, where carbon dioxide

fi xation occurs. Thylakoids are free in plastid stroma, isolated or in groups

of two or more thylakoids, called lamellae. In red algae, thylakoids are not

grouped, and they are associated with granules, the phycobilisomes, where

phycobiliproteins (mainly phycoerythrin and phycocyanin) are contained.

In the remaining groups of algae, thylakoids are gathered in groups. In

golden brown algae, thylakoids form packs of three, which are surrounded

by a band of three thylakoids or a girdle lamella (Fig. 1c). In some green

6 Marine Algae

algae, clusters of thylakoids are interconnected by other thylakoids forming

compact stacks known as grana, such as in land plants. Chlorophylls and

carotenoids are associated with thylakoids. Carotenoids, as previously

mentioned for phycobiliproteins, constitute auxiliary pigments, and there

are two types: free oxygen or hydrocarbon carotenes and their oxygenated

derivatives called xanthophylls.

In certain groups of algae, the chloroplast is surrounded by one or two

additional membranes. When there are two additional membranes, the

innermost membrane represents the plasma membrane of the alga that was

phagocytized, while the outer membrane often has attached ribosomes and

is considered to have originated from the endoplasmic reticulum. In these

cases, the outer membrane also surrounds the nucleus, and microtubules and

vesicles with storage products can be found in between the two membranes,

leading us to think that these chloroplasts may have a endosymbiotic

origin, so-called secondary endosymbiosis (Fig. 2). When ribosomes are

only present on a third membrane, as in dinofl agellates, it is interpreted

that the host plasma membrane was destroyed upon phagocytosis. Species

of Cryptophyta present a different situation, because their chloroplasts

have important remnants of genome present in phagocytosed alga, the

nucleomorph. In Chlorarachniophyta and Glaucophyta, the chloroplast has

four membranes and the outermost membrane lacks associated ribosomes,

suggesting that it was originated by a digestive vacuole.

Chloroplasts contain circular DNA without histones and 70S ribosomes.

They often exhibit electron-dense areas, called pyrenoids, consisting of

polypeptides with enzymatic properties. They have been associated with

carbon dioxide fi xation, since reserve products such as starch tend to

accumulate around them. Another structure that can be found in many

unicellular algae is the stigma or orange or red colored eyespot, consisting

of packed carotenoids. Eyespot is considered to be related to phototaxis

and is associated with photosensitive proteins. Eyespot seems to be a

shading device to the true photoreceptor. In some groups of algae, such

as euglenophytes and dinofl agellates, the stigma is located outside the

chloroplast. The nucleus is surrounded by a double membrane, called

the nuclear membrane, which contains DNA, proteins, small amounts

of RNA and the bulk substance or nucleoplasm. The nuclear membrane,

derived from the endoplasmic reticulum of the cell, is perforated by

numerous pores. DNA is organized into chromosomes which are not

visible during interphase, as in most plants and animals with the exception

of euglenophytes, dinofl agellates and cryptophytes, in which DNA is

condensed in chromosomes during interphase. The number of chromosomes

in algae varies greatly from 2 to over 80.

Many algae, or their reproductive cells, are motile by fl agella. The

fl agellum is an axoneme, consisting of nine pairs of microtubules that encircle