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Microalgae in Health and Disease Prevention

Microalgae in Health and Disease Prevention

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Microalgae in Health and Disease Prevention

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Microalgae in Health and Disease Prevention is a comprehensive reference that addresses the historical and potential use of microalgae, its extracts, secondary metabolites, and molecular constituents for enhancing human health and preventing diseases. Each chapter features an overview, and the book includes coverage of microalgae biology, harmful algae, the use of microalgae in alcohol and food, and as sources of macronutrients, micronutrients, vitamins, and minerals. The historical use of microalgae, in addition to its potential use as a nutraceutical and cosmeceutical, is also addressed.

The book provides coverage of relevant, up-to-date research as assembled by a group of contributors who are dedicated to the advancement of microalgae use in health, diet and nutrition.

  • Discusses research findings on the relationship between microalgal diet, nutrition and human health
  • Presents the medicinal, anti-allergic and psychoactive properties of microalgae
  • Identifies toxic and harmful microalgae
  • Addresses microalgal lipids, proteins and carbohydrates
Lansat:
Jun 29, 2018
ISBN:
9780128114063
Format:
Carte

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Microalgae in Health and Disease Prevention - Academic Press

Microalgae in Health and Disease Prevention

Editors

Ira A. Levine

Natural and Applied Sciences, University of Southern Maine, Lewiston, ME, United States

Joël Fleurence

University of Nantes, Nantes, France

Table of Contents

Cover image

Title page

Copyright

Dedication

List of Contributors

About the Editors

Chapter 1. Algae: A Way of Life and Health

Chapter 2. Society and Microalgae: Understanding the Past and Present

1. Introduction

2. Emergence of Photosynthesis, Microalgae, Plants, and Humans

3. Algae in Human Nutrition

4. Microalgae Biofertilizers and Inoculants for Crop Production

5. Potential for Renewable Algal Biofuels and Industrial Chemicals

6. Carbon Sequestration by Microalgae, Its Reversal, and the Fossil-Fuel Driven Economy

7. Nutrient Removal From Wastewaters

8. Harmful Algal Blooms and Societal Impact

9. Emerging Products and Processes

10. Concluding Remarks

Chapter 3. Biology of Microalgae

1. Introduction

2. Habitats and Growth Forms

3. Plastids and the Evolution of the Algae

4. Cell Coverings

5. Nutrition

6. Selected Taxa and Species of Particular Interest

7. Microalgae as Environmental Indicators

8. Algal Blooms and Harmful Algae

9. Chemically Mediated Interactions and Allelopathy

10. Summary

Chapter 4. Microalgal Systematics

1. Introduction

2. The Algae

3. Microalgae and Human Health

Chapter 5. Lipids From Microalgae

1. Introduction

2. Lipids in Microalgae

3. Abiotic Factors and Responses in Lipid Synthesis: Example of Diatoms

List of Abbreviations

Chapter 6. Carbohydrate Diversity in Microalgae: A Phylogenetically Arranged Presentation

1. Introduction

2. Evolutionary History and Groups Presented

3. Why This Classification Strategy Works, an Example

4. Cyanophytes

5. Lower Archaeplastida

6. Higher Archaeplastida

7. Cryptomonads

8. Dinophytes

9. Haptophytes

10. Unicellular Heterokonts

11. Phaeophytes

12. Chlorarachniophytes

13. Euglenophytes

14. Biomedical Applications

15. Conclusion and Potential for Bioprospecting Carbohydrates

Chapter 7. Proteins and Pigments

1. Introduction

2. Pigments

3. Proteins

4. Conclusion and Future Trends

Chapter 8. Minerals and Trace Elements in Microalgae

1. Introduction

2. Mineral Functions

3. Mineral Composition of Microalgae

4. Requirements for Minerals by Humans

5. Mineral Accumulation in Microalgae and Downstream Toxicity

Chapter 9. Microalgae in Medicine and Human Health: A Historical Perspective

1. Introduction

2. Historical Uses of Microalgae for Human Health (before 1900)

3. The Rise of Microalgae for Human Health

4. Conclusions

Chapter 10. Microalgae in Human Health: Interest as a Functional Food

1. Introduction

2. Nutritional Aspects of Microalgae

3. Potential of Microalgae in Cardiovascular Disease Prevention

4. Anti-inflammatory and Immunomodulatory Activity

5. Antiviral Activity

6. Antimicrobial Activity

7. Potential Activities of Microalgae Against Cancer

8. Miscellaneous

9. Conclusion

Chapter 11. Microalgae and Alcohol

1. Introduction

2. Microalgal Species Suitable for Bioethanol Production

3. Conclusions

Chapter 12. Anticancer, Antiviral, Antibacterial, and Antifungal Properties in Microalgae

1. Introduction

2. Anticancer Activity

3. Antiviral Activity

4. Antibacterial Activity

5. Antifungal Activity

6. Conclusion and Prospects

Chapter 13. Microalgae and Toxins

1. Introduction

2. Dinoflagellates

3. Diatoms: The Pseudo-nitzschia Genus and Their Phycotoxins

4. Emerging Marine Phycotoxins

5. Regulatory Aspects of Phycotoxins

Chapter 14. Antiallergic and Allergic Properties

1. Introduction

2. Antiallergic and Anti-inflammatory Properties

3. Allergic and Inflammatory Properties

4. Environmental Conditions

5. Development of Novel Antiallergic Drugs From Microalgae

6. Conclusion

Chapter 15. Microalgal Application in Cosmetics

1. Introduction

2. Generalities About Cosmetics

3. Microalgae Treatment for Cosmetic Applications

4. Microalgae as a Source of Active Ingredients

5. Microalgae as a Source of Additives

6. Conclusion

Chapter 16. Psychoactive Properties of Microalgae

1. Introduction

2. Phytocompounds That Have Psychoactive Potentials

3. Balancing the Benefits and Side Effects of Microalgae

4. Microalgae—New Neurological Therapeutic Treatment for Alzheimer Disease

5. Conclusion

Index

Copyright

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Notices

Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary.

Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility.

To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein.

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A catalogue record for this book is available from the British Library

ISBN: 978-0-12-811405-6

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Dedication

To Doctor, Director, and Manager Levines for all the nachas you bring me. To Laurie, my guiding light and best friend and to baby Ari Makai, the 8th generation of an only son of an only son, keep our name with pride and integrity. You all fill my life with hope and love.

To George Schumacher, John Kingsbury, Harold Humm, Maxwell Doty, and Isabella Abbott, thank you for the lessons learned.

To the beautiful game of rugby without which I would not have met my wife, made and kept life-long friends, traveled the world and became a Phycologist. Otherwise I would have been an unhappy medical doctor.

Ira A. Levine

To Alicia from her grandfather, who is happy to see her beautiful smile; to his mother Cynthia and father Julien, who are young researchers devoted to their passions; and to Simon, my youngest son, ingenious engineer. I would like to dedicate this with all my pride and love for the happiness you bring to my life.

Joël Fleurence

List of Contributors

Zouher Amzil,     IFREMER, Nantes, France

Jean-Marie Bard

Faculté des Sciences Pharmaceutiques et Biologiques, EA2160 – Mer Molécules Santé (MMS) – IUML (Institut Universitaire Mer et Littoral) – FR 3473 CNRS – Centre de Recherche en Nutrition Humaine Ouest, Nantes, France

Institut de Cancérologie de l’Ouest, Centre René Gauducheau, Saint-Herblain, France

Michael A. Borowitzka

Murdoch University, Murdoch, WA, Australia

OzAlgae, Cygnet, TAS, Australia

Nathalie Bourgougnon,     Université Bretagne Sud, Vannes, France

Intan C. Dewi,     Le Mans Université, Le Mans, France

Amandine M.N. Caruana,     IFREMER, Nantes, France

Yusuf Chisti,     Massey University, Palmerston North, New Zealand

Laurence Coiffard,     University of Nantes, Nantes, France

Céline Couteau,     University of Nantes, Nantes, France

Aurélie Couzinet-Mossion,     University of Nantes, Nantes, France

Justine Dumay,     Université de Nantes, Nantes Cedex 3, France

Charlotte Falaise,     Le Mans Université, Le Mans, France

Joël Fleurence,     University of Nantes, Nantes, France

Joe M. Fox

Texas A&M University-Corpus Christi, Corpus Christi, TX, United States

Texas A&M AgriLife Research, Corpus Christi, TX, United States

Taejun Han

Ghent University Global Campus, Incheon, Republic of Korea

Incheon National University, Incheon, Republic of Korea

Claire Hellio,     Universitaire Européen de la Mer (IUEM) - UBO – UEB Technopôle Brest-Iroise, Plouzané, France

Matthew L. Julius,     St. Cloud State University, St. Cloud, MN, United States

Jang K. Kim,     Incheon National University, Incheon, Republic of Korea

Ira A. Levine,     University of Southern Maine, Lewiston, ME, United States

Michael W. Lomas,     National Center for Marine Algae and Microbiota (NCMA), East Boothbay, ME, United States

Virginie Mimouni,     University of Le Mans, Le Mans-Laval, France

Michèle Morançais,     Université de Nantes, Nantes Cedex 3, France

Jean-Luc Mouget,     Le Mans Université, Le Mans, France

Hassan Nazih,     Faculté des Sciences Pharmaceutiques et Biologiques, EA2160 – Mer Molécules Santé (MMS) – IUML (Institut Universitaire Mer et Littoral) – FR 3473 CNRS – Centre de Recherche en Nutrition Humaine Ouest, Nantes, France

Jihae Park,     Ghent University Global Campus, Incheon, Republic of Korea

P.D. Rajakumar,     Imperial College London, Kensington, United Kingdom

Julianne P. Sexton,     National Center for Marine Algae and Microbiota (NCMA), East Boothbay, ME, United States

Lionel Ulmann,     University of Le Mans, Le Mans-Laval, France

Gaëtane Wielgosz-Collin,     University of Nantes, Nantes, France

Charles Yarish,     University of Connecticut, Stamford, CT, United States

Paul V. Zimba,     Texas A&M University-Corpus Christi, Corpus Christi, TX, United States

About the Editors

Dr. Ira A. Levine, Ph.D. is a tenured Professor of natural and applied sciences at the University of Southern Maine, President and Board Chair of the Algae Foundation, Executive Director of Professors Beyond Borders, and the CEO of Algal Aquaculture Professionals, LLC. Dr. Levine was: selected as the Trustee Professor of University of Southern Maine for 2017–18. He was awarded the U.S. State Department’s distinguished Fulbright New Century Scholar in 2009–10 and Chair Fulbright in 2016–17. He was a visiting Professor of biology at Duke University in 2007–08. Dr. Levine combines 33 years of basic and applied research in physiological ecology and cultivation of algae, algal farm management, and aquaculture engineering. His farming experience includes open-ocean and pond cultivation in Canada, China, Indonesia, Japan, Malaysia, Philippines, and USA (Hawaii, Florida, and Maine). Current efforts include algal cultivar enhancement for biofeeds, human nutraceuticals, and cosmeceuticals, fine chemicals, and algal-based biofuels.

Dr. Joël Fleurence, Ph.D., is a Professor of Marine Biology and Biochemistry at the University of Nantes. He is one of the two Directors of the Research Laboratory Sea, Molecules, Health. He is a member of the University National Council since 2007 and was elected President of the section Biology of organisms since 2017. He is a senior scientist and an international expert on the seaweed valorization (120 international publications including patents). In 1985, he began his research career in the pharmaceutical industry in the French Company Roussel Uclaf. In 1990, he was recruited by the Institute of Valorization of Seaweeds (CEVA, Brittany, France) to lead researches about the chemical composition and nutritional properties of macroalgae. Professor Fleurence has participated in the establishment of the French regulation on marine algae used as sea vegetables. In 1994, he arrives as a head of laboratory Proteins and Quality at IFREMER (Research French Organism for the Sea Exploitation) and develops research on the nutritional properties of seaweed protein for use in human or animal food. Since 2002, he is a Professor at the University of Nantes and leads research on the development of seaweed uses as protein or pigment sources for the industry.

Chapter 1

Algae

A Way of Life and Health

Ira A. Levine     University of Southern Maine, Lewiston, ME, United States

Abstract

Microalgae are responsible for nearly half the global production of oxygen via photosynthesis; they can improve one's general health, cure acute illness, or kill a person; this is the paradox of microalgae. Algae in general and the microalgae (phytoplankton) in particular are a diverse assemblage of plantlike predominantly aquatic, unicellular, multicellular, or colonial; photosynthetic; chlorophyll a containing; two domain occupying (Eukaryota and Bacteria) organisms. The algae can range in size from 0.5  μm in diameter (Synechococcus) to ∼30  m (Macrocystis). There are approximately 20,000 and 41,000 described species of macroalgae and microalgae, respectively. The algae are classified depending on photosynthetic pigment content, carbohydrate food reserve, cell wall components, and flagella construction and orientation. Microalgae, an eclectic group, have evolved over the last 2500  million years (1600–1900  million years older than the seaweeds), occupy a large variety of habitats, including the atmosphere, mountain tops, and 200–300  m below the surface of the earth.

Utilization of the microalgae range from folk medicine to aquaculture feeds. The diverse applications of microalgae for medicinal purposes include: antifungal, anticancer, antiviral, antioxidant, antiallergic, anti-inflammatory, antimicrobial, and the reduction of biofilms. Alternatively, microalgae also produce potent toxins, allergens, and irritants that cause mild reactions like skin rashes to serious threats, like loss of life.

The editors have assembled a group of contributors, dedicated to the advancement of algae, experts in their fields, endeavoring to bring microalgae and their role in health and disease prevention to a diverse group of readers.

Keywords

Algae; Health and disease; Microalgae; Phytoplankton

Chapter Outline

References

Vilor Alga (translated as more vile or worthless than algae) wrote Virgil, the Latin poet, in 30 BCE. Civilizations were aware of the role of algae in human health long before Virgil. The use of microalgae dates back 1000  years in Asia and 700  years by the Aztecs, approximately 3700  years after the first documented use of seaweeds. Contrary to the use of microalgae as a functional food or health tonic, there are historical indications of algal-based pathogens, including: The first plaque visited upon the Pharaoh of Egypt in the Bible’s book of Exodus, which could be considered a reference to a red tide; the Caribbean in the 1500’s (Halstead, 1978); and the South Pacific in 1606 by the Spanish explorer de Quinos (Mills and Passmore, 1988) with symptoms brought on by ingestion of shell or finfish, direct skin contact, and/or respiratory inhalation.

Microalgae (phytoplankton) are a diverse assemblage of plantlike, predominantly aquatic, unicellular, multicellular, or colonial forms; photosynthetic; chlorophyll a containing organisms found in the atmosphere, on mountain tops, and 200–300  m below the ocean-air interface. The microalgae are evolutionarily diverse occupying two domains, Eukaryota and Bacteria, and include, but not limited to the, cyanobacteria (blue-green algae), Charophyta (chara), Chlorophyta (green), Rhodophyta (red), Ochrophyta (brown), Glaucophyta, Euglenophyta, Cryptophyta, Chrysophyta, Bacillariophyceae (diatoms), and Dinophyceae (dinoflagellates). The approximately 41,000 described microalgal species are segregated by photosynthetic pigment content, carbohydrate food reserve, cell wall components, and flagella construction and orientation. This eclectic group has evolved over the last 2500  million years (1600–1900  million years older than the seaweeds), occupying a variety of ecological niches, that is, planktonic, benthic (growing in sand, mud, soil), epilithic, epiphytic (growing on other algae, seagrasses, and trees), symbiotic relationships with fungi and invertebrates, atmospheric, and in rare occasions, parasitic. There are additional groups of algae, which can form biofilms, colonial formations, mats, and turfs. The term microalgae will include both the eukaryotic and cyanobacterial forms for the sake of discussion in this chapter. Despite the total number of described microalgae, perhaps only a few hundred species have been investigated thoroughly, only several dozens of which are fully understood, with their nutritional, health, pathogenic, or commercial potential truly delineated. There is much work to be done with this eclectic group before we can fully appreciate the value of microalgae in health and disease prevention. The algae play an essential role as the foundation of all aquatic food webs and in the production of more than half of our globe’s oxygen. Additionally, via photosynthesis and nitrogen fixation, microalgae act as major components of the carbon (Falkowski and Raven, 2007) and nitrogen cycles (Fowler et al., 2013), respectively.

As algae in general and microalgae in particular have played an ever increasing role in humans’ diet, health, and well-being, their utilization and product development have rapidly expanded our appreciation for the diverse phytochemicals that the algae produce (Table 1.1). Humans augment traditional medical practices by incorporating nutraceuticals and supplements, thus acknowledging the relationship between health and diet. Microalgae have been a significant component of mainstream dietary supplements for the past generation. The most common commercially exploited microalgal genera are Arthrospira (Spirulina), Chlorella, Dunaliella, and Haematococcus. Benefits include: immune system enhancement, reduction in viral infections and cancer onset, pre- and probiotic effects, increase in hemoglobin concentrations, and the reduction in blood sugar levels and bacterial populations. Historically, Chlorella and plankton soup were utilized as far back as 1942, to aid leprosy patients by supporting increase in weight, energy, and general health (Barrow and Shahidi, 2008). Additionally, microalgal-sourced, omega 3 and 6 long chain polyunsaturated fatty acids (PUFA’s) are utilized for neurological and cardiac development, and support decrease in skin diseases, rheumatism, coronary heart disease, hypertension, cancer, and cholesterol levels (Mata et al., 2010). Haematococcus pluvialis produces the pigment astaxanthin, which is recently approved as a dietary supplement and is the feed additive responsible for the reddish pink flesh of aquacultured salmon. Astaxanthin ingestion has been linked to antibody production; antitumor and anti-inflammatory activity; inhibition of colon, bladder, liver, mammary, and oral cancers; decreasing risk of Parkinson’s and Alzheimer’s diseases; and improvement in cardiovascular health (Mata et al., 2010).

Table 1.1

Liu, R., 2004. Potential synergy of phytochemicals in cancer prevention: mechanism of action. Journal of Nutrition 134, 3479–3489; Prakash, D., Gupta, C., Sharma, G., 2012. Importance of phytochemicals in nutraceuticals. Journal of Chinese Medicine Research and Development 1 (3), 70–78 as adopted from Raposo, M., de Morais, A., 2015. Microalgae for the prevention of cardiovascular disease and stroke. Life Sciences 125, 32–41.

Through adaptive evolution and metabolic diversity, microalgae have developed a variety of bioactive compounds. While many of these compounds have biomedical properties that benefit human health, few act as neurological and gastrointestinal toxins. Curiously, freshwater microalgal-based toxins are produced primarily by cyanobacteria, whereas marine microalgal-based toxins are produced by dinoflagellates and diatoms. The toxins tend to be heat-stable, tasteless, odorless, resistant to acids, and cooking has no effect on them (Backer et al., 2004). Table 1.2 includes the toxins, source algae, route of acquisition, and clinical manifestation.

The use of microalgae, especially Chlorella and Arthrospira, as dietary supplements must be tempered due to potential contamination from cultivation, harvesting, processing, and/or storage stages of supplement preparation. Contaminations can include pathogenic alternative species, heavy metals, cyanotoxins, and inorganic arsenic. Quality control and quality assurance best practices are needed to reduce or eliminate potential contamination sources, and the purchase of supplements should be restricted to highly qualified and certified producers, packagers, and distribution concerns (Rzymski et al., 2015).

With the continued use and development of algal-based supplements, additional clinical studies and precautions should be undertaken in the best interest of the public. Rzymski et al. (2015) list a few best practices to follow:

1. It is not advisable to use Chlorella and Spirulina-based products simultaneously.

2. Use of commercial microalgae-based products should be avoided in individuals suffering from renal failure and susceptible to Al compounds due to potentially high level of Al contamination in these supplements.

3. Use of microalgae-based products should be avoided in individuals suffering from autoimmune diseases, as a relapse of symptoms can occur.

4. Use of microalgae-based products of unknown origin should be avoided.

5. Use of microalgae-based products in infants and children should be limited.

6. All microalgal-based products should be subject to quality screening and safety assessments performed routinely by independent agencies prior to registration.

7. All microalgae-based products characterized by detectable cyanotoxin content and significant levels of Al and other toxic metals should be systematically eliminated from the market.

Drug discovery over the past 70  years has resulted in nearly 28,000 compounds isolated from marine organisms, only 7 of which have been approved for human pharmaceutical use. The drug approval pipeline has an additional 26 in phase I or II trials. The candidates include 23 anticancer, 2 schizophrenia and Alzheimer’s, and 1 chronic pain treatments (Lauritano et al., 2016). Most of the marine drug discoveries originated in sponges or ascidians which are difficult to culture and whose standing stocks do not represent a commercial source of finished drug source material. The ease of collection, isolation, identification, cultivation, harvesting, and extraction of microalgae and their metabolites represent an attractive alternative research group. Algae’s evolution over the course of 2500  million years, its diversity, and ability to inhabit extreme environments have resulted in novel defense, communication, and survival techniques, adding to their human drug and nutraceutical potentiality (Lauritano et al., 2016). Numerous pharmacological activities have been reported and tested (Tables 1.3 and 1.4) such as: allelopathic, anti-inflammatory, anticancer, antiobese, antidiabetic, antiangiogenic, antimalarial, antioxidant, antibacterial, antiviral, and growth inhibiting properties (Gastineau et al., 2014; Guedes et al., 2013; Mimouni et al., 2012; Nigjeh et al., 2013; Patterson et al., 1990a,b; Peng et al., 2011; Samarakoon et al., 2013). However, one note of caution is that drug discovery in microalgae is a function of cultivation of environmental regimes resulting in metabolic plasticity (Lauritano et al., 2016). Metabolite production and bioactivity levels vary as a function of habitat and seasonality. Primary and secondary metabolites production and concentration are a function of: growth phase (Vidoudez and Pohner, 2012), clones (Gerecht et al., 2011), light (Depauw et al., 2012), temperature (Huseby et al., 2013), culturing media (Alkhamis and Qin, 2015), grazing pressure (Pohnert, 2002), extraction method (Juttner, 2001), and many other factors (Chen et al., 2011). An example of metabolic plasticity is the elevated inhibition of biofilm formation by Leptocylindrus danicus and L. aporus, and anticancer activity by Skeletonema marioni in nitrogen and phosphorus starved growth media.

The progress of phycology, the study of algae, within the public consciousness can be summarized by a seminar given by the author at Middlebury College, Middlebury, Vermont, USA in March 2010, The Road from Science Geek to Being Cool, Algal Physiological Ecology: a Global Economic Development Engine. As algae and algal-based biofuels became a research and development priority in the United States during the 21st century, the once obscure field is now experiencing a surge of notoriety. If studying algae, previous to the renewed interests, was held in such disregard or benign neglect, then why would anyone dedicate his or her life to algae? Phycology has a long history of remarkable, dedicated scientists and lay practitioners who have advanced our algal-based knowledge through their tireless field and laboratory efforts. Massive algal collections were assembled at universities (e.g., University of Texas, Austin, Texas), research institutions (e.g., Bigelow Laboratory for Ocean Sciences, Boothbay, Maine) and museums (e.g., Bishop Museum, Honolulu, Hawaii). Meticulous anatomical, reproductive, and systematic treatises were published expanding our body of knowledge. Biotechnological methodologies were incorporated into current molecular genomic, ultrastructure, physiological ecology, and biochemical studies advancing our understanding of the biology, ecology, systematics, and commercial value of the algae. Algae represent a field of study that is far from the mainstream science. Phycologists have enjoyed their life’s work in relative obscurity until the recent interest in algae farming (Cyanotech), algae as a healthy food (blue-green manna), feed, medicine, and biofuel (Exxon). Algae enjoy the focus and funding so as to move microalgae and its place in health and disease prevention to the forefront in research. The editors have assembled a group of contributors dedicated to the advancement of algae, experts in their fields, endeavoring to bring seaweeds and their role in health and disease prevention to a diverse group of readers. Below is a poem dedicated to algae:

Table 1.2

Table 1.3

Adopted from Raposo M., de Morais A. Microalgae for the prevention of cardiovascular disease and stroke. Life Sciences 125, 2015, 32–41.

Table 1.4

Adopted from Raposo M., de Morais A. Microalgae for the prevention of cardiovascular disease and stroke. Life Sciences 125, 2015, 32–41.

The Biology of Algae by R.A. Lewin (1981). Phycol. Newsletter 7:1

The biology of algae is a duty, or a task,

That consumes the better portion of your time

In the sampling of waters from an ocean, or a flask,

Or a snow-field, or a gutter-full of slime.

You get cold, and wet, and grubby; you get dusty, hot, and dry;

You get dian dejected, and defied;

But you’ll find that, if you’re lucky-if you’re good-and if you try,

You can do a little science on the side.

The biology of algae is a pastime, or an art,

That embodies a diversity of skill:

How to mend a pH meter which has somehow come apart,

Or to regulate a microscope or still;

How to edit a proposal, or a chapter of a book;

How to float upon the academic tide;

How to teach a fellow creature how to speak, or how to cook,

And a little bit of science on the side.

The biology of algae is a virtue, or a vice,

That entails some tricky searching of the soul.

It involves the growth of fishes, and the harvesting of rice,

And pollution, and the origins of coal.

It may get us into trouble; it may get us into space;

Its dilemmas are as long as they are wide.

It involves some moral judgements on the future of our race –

And a little bit of science on the side.

References

Alkhamis Y, Qin J. Comparison of pigment and proximate compositions of Tisochrysis lutea in phototrophic and mixotrophic cultures. Journal of Applied Phycology. 2015;28:35–42.

Backer L, Fleming L, Rowan A, Baden D. Epidemiology and public health of human illnesses associated with harmful marine phytoplankton. Monograph on oceanographic methodology. In: 11: Manual on Harmful Microalgae. 2004:723–750.

Barrow C, Shahidi F. Marine Nutraceuticals and Function Foods. CRC Press; 2008.

Ben-Amotz J, Levy Y. Bioavailability of a natural isomer mixture compared with synthetic all trans β-carotene in human serum. American Journal of Clinical Nutrition. 1996;63:729–734.

Bertolin T.E, Pilatti D, Giacomini A.C.V.V, Bavaresco C.S, Colla I.M, Costa J.A.V. Effect of microalga Spirulina platensis (Arthrospira platensis) on hippocampus lipoperoxidation and lipid profile in rats with induced hypercholesterolemia. Braz. Arch Biol Technol. 2009;52(5):1253–1259.

Bobrov Z, Tracton I, Taunton K, Mathews M. Effectivenss of Whole Dried Dunaliella Salina Marine Microalgae in the Chelating and Detoxification of Toxic Minerals and Heavy Metals DetoxPaper 100308.pdf. 2008. .

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Chapter 2

Society and Microalgae

Understanding the Past and Present

Yusuf Chisti     Massey University, Palmerston North, New Zealand

Abstract

The societal impact of microalgae is discussed in this chapter. Evolution of microalgae and cyanobacteria impacted the global environment to make human life possible. Over the years, microalgae removed huge tonnages of carbon from the atmosphere to sequester it in mineral deposits and fossilized carbon. Microalgae gave rise to higher plants, the basis of all terrestrial ecosystems, and may have influenced the development of hominid brain. As the primary producers in the seas, microalgae are the source of all our seafood. Nitrogen fixing cyanobacteria contributed to productivity of terrestrial plants long before mankind was able to chemically fix nitrogen. Being primary producers reliant on sunlight, water and carbon dioxide, microalgae together with higher plants may be the future basis of a sustainable economy. Materials now obtained from petroleum may be sustainably produced in the future using microalgae. Microalgae contribute to treating wastewaters, provide diverse useful products and emerging products, and, sometimes, adversely impact human life.

Keywords

Aquaculture; Biofertilizers; Biofuels; Carbon sequestration; Harmful algal blooms; Human nutrition; Industrial chemicals; Microalgae evolution; Societal impact; Wastewater treatment

Chapter Outline

1. Introduction

2. Emergence of Photosynthesis, Microalgae, Plants, and Humans

3. Algae in Human Nutrition

3.1 Macroalgae (Seaweeds)

3.2 Microalgae and Cyanobacteria

3.3 Microalgae and Aquaculture

4. Microalgae Biofertilizers and Inoculants for Crop Production

5. Potential for Renewable Algal Biofuels and Industrial Chemicals

6. Carbon Sequestration by Microalgae, Its Reversal, and the Fossil-Fuel Driven Economy

7. Nutrient Removal From Wastewaters

8. Harmful Algal Blooms and Societal Impact

9. Emerging Products and Processes

10. Concluding Remarks

References

1. Introduction

Microalgae are a diverse group of photosynthesizing eukaryotic microorganisms. Another large group of photosynthesizing prokaryotes, the cyanobacteria, is often discussed together with microalgae. This convention will be followed here, although the two groups of microorganisms are quite distinct. The exact number of algal species is unknown (Guiry, 2012). Estimates vary from 45,000 to over 100,000 species. Many species of freshwater cyanobacteria and microalgae today exist in widely dispersed and disconnected water bodies. The commercially used green freshwater microalga Haematococcus pluvialis (Chlorophyceae), for example, has been isolated from every continent except Antarctica. The mechanisms behind the wide dispersal of microalgae are not entirely clear. Contributing factors likely include: flooding events; transport by surface waters; windblown spray and dust harboring dormant cysts; and dispersal by waterfowl (Coleman, 1996) and aquatic insects.

Public perception of algae is often one of nuisance (Chapman, 2013)—in swimming pools; eutrophicated lakes, rivers, and coastal waters (see Section 7); harmful algal blooms; and algae-linked shellfish poisonings (see Section 8). This notwithstanding, algae are perhaps the historical reason for our existence (see Section 2) and remain vital to our survival. For example, nearly 50% of all oxygen released into the atmosphere is linked to oceanic photosynthesis ascribed almost exclusively to various algae. Algae are the ultimate source of much of our seafood (Section 3.2). Although here we are concerned with microalgae, another group of large algae, the seaweeds or macroalgae, are perhaps more visible (see Section 3.1). Although macroalgae have been used by humans since at least 2700 BC as food, medicine, fertilizers, and cosmetics, commercial production of both macroalgae and microalgae is relatively recent.

Microalgae and cyanobacteria contribute to human society in diverse ways as discussed in this chapter. While their economic potential is immense, they have a much bigger ecological role in assuring survival of life on Earth. Established and emerging products derived from them have been extensively discussed in the literature (Kay, 1991; Benemann, 1992; Borowitzka, 1992, 1995, 2013; Lee, 1997; Gantar and Svirčev, 2008; Gershwin and Belay, 2008; Chacoón-Lee and González-Mariño, 2010; Gallardo-Rodríguez et al., 2012; Posten and Walter, 2012a,b; Sharma et al., 2014; Specht and Mayfield, 2014; Gimpel et al., 2015; Rasala and Mayfield, 2015; Bux and Chisti, 2016; Raja et al., 2016; Wells et al., 2017). A summary of products and potential products is shown in Fig. 2.1. Algae and cyanobacteria are the primary producers in the sea. Production of all seafood in nature depends on algae. On land, plants descended from algae are the source of all our food and fodder. All life can be ultimately traced to algae and their predecessors.

Figure 2.1  Some products and potential products from microalgae and cyanobacteria.

2. Emergence of Photosynthesis, Microalgae, Plants, and Humans

Earth came into being around 4.5  billion years ago. The early atmosphere contained a lot more carbon dioxide than we have today, but little free oxygen. The first lifeforms emerged around 3.5–4  billion years ago. Photosynthesis had evolved by 3.4  billion years ago but early photosynthesizing microorganisms did not produce oxygen. Oxygen generating photosynthesis evolved prior to 2.4  billion years ago, likely as early as 3  billion years ago (Kaufman, 2014). Around 2.4  billion years ago, the Earth acquired a breathable atmosphere as a consequence of oxygen evolving microbial photosynthesis. Oxygen evolving photosynthesis, or oxygenic photosynthesis, uses sunlight to covert inorganic carbon dioxide and water to oxygen and organic carbohydrates. The latter, together with other inorganic nutrients, are used to make the structural chemicals that compose the bodies of microalgae, cyanobacteria, and higher plants.

The early photosynthesizing microbes were the immediate predecessors of today’s cyanobacteria and microalgae. Eukaryotic microalgae evolved between 1 and 2  billion years ago. Macroalgae evolved later, possibly around 1  billion years ago. Based on fossil evidence, at least four types of microalgae moved from water to land around 465  million years ago. These were the freshwater green algae known as charophytes; the freshwater chlorophytes chlorophyceae and trebouxiophyceae; and the saltwater trentepohiales. Ancestors of only the trentepohiales, a group of 60 terrestrial algal species that colonize rocks and tree bark, emerged from saltwater; all the rest came from freshwater. Of the algae that came ashore, only the charophytes evolved the necessary complexity to progress to higher plants (McCourt et al., 2004; Delwiche and Cooper, 2015; Gerrienne et al., 2016; Harholt et al., 2016). The earliest land plants (bryophytes; liverworts, hornworts, and mosses) most resembled the charophyte orders coleochaetales and charales. Genetic evidence concurs with a single common lineage for all the multicelled land plants (Graham, 1996). Descendants of the other algae that originally colonized land continue to exist today mostly as subaerial algae, that is, the algae that typically grow exposed to air.

The current oxygen-rich atmosphere produced via oxygenic photosynthesis enabled evolution of oxygen-breathing lifeforms, including mammals. Mammals, the group of warm-blooded animals to which we belong, evolved some 220  million years ago but hominids (the group including all modern and extinct great apes) did not appear until around 7  million years ago. Humans appeared only around 200,000  years ago.

Algae are believed to have had a role in emergence of humans from our hominid ancestors. The size and capacity of human brain distinguish us from the other hominids. Brain is mostly fat (∼60% fat). Nearly 20% of the brain fatty acids consist of the omega-3 fatty acid docosahexaenoic acid (DHA, C22:6n3, C22H32O2) and the omega-6 fatty acid arachidonic acid (AA, C20:4n6, C20H32O2). These fatty acids are most readily accessible through a diet rich in DHA and AA. Hominid diets rich in aquatic foods with plentiful microalgae-derived DHA and AA are believed to have contributed to the evolution of human brain (Crawford et al., 1999; Joordens et al., 2009; Cunnane and Stewart, 2010; Bradbury, 2011; Cunnane and Crawford, 2014). DHA, found mainly in aquatic animals, originates in microalgae and is bioaccumulated through the food chain. AA has other potential sources (e.g., oil seeds, vegetable oils), but aquatic animals were likely the most readily available source to our hominid ancestors. (DHA and AA can be produced in the body from dietary intake of the essential fatty acids linoleic acid (LA, C18:2n6, C18H32O2) and α-linolenic acid (α-LNA, C18:3n3, C18H30O2) found in oil seeds and vegetable oils.) In view of their importance, DHA and AA are added to nearly all baby formula. DHA occurs in fish oil, but most of the DHA used in infant formula is sourced from Crypthecodinium cohnii (Wikfors and Ohno, 2001; Mendes et al., 2009) and the Thraustochytrid Schizochytrium sp. (Winwood, 2013). Heterotrophic culture is used in producing DHA.

3. Algae in Human Nutrition

3.1. Macroalgae (Seaweeds)

Macroalgae are the basis of a large industry with a global output value exceeding $6  billion. Seaweeds are grown commercially in coastal waters in more than 30 countries. They are a source of food and other valuable products. Global annual seaweed production is about 10 million tons (fresh weight). The kelp Saccharina japonica is produced most widely for food. Other important commercial species are the red alga, Pyropia yezoensis, nori in Japanese, and the brown alga, Undaria pinnatifida, wakame in Japanese. In addition, polysaccharides (e.g., agars, carrageenans, alginates) or phycocolloids, obtained from macroalgae are widely used as food thickeners and texture modifiers (Wikfors and Ohno, 2001). Macroalgae for food and hydrocolloids are cultivated, but wild harvested biomass is also used in these applications. Production of macroalgae for food and biopolymers is further discussed elsewhere (Wikfors and Ohno, 2001; McHugh, 2003; Bixler and Porse, 2011). Seaweed farming has impacted economic wellbeing of numerous coastal communities.

3.2. Microalgae and Cyanobacteria

Only the green microalga Chlorella and the cyanobacteria Arthrospira (Spirulina) and Nostoc are used as food. Chlorella is poorly digested and therefore cannot be used as a bulk human food (Wikfors and Ohno, 2001). Several other microalgae are a source of food additives (e.g., pigments and colorants) and nutraceuticals. The marine microalga Dunaliella is used to produce the orange-red pigment β-carotene (provitamin A). The green freshwater microalga Haematococcus pluvialis is used in commercial production of astaxanthin, the red pigment that is responsible for red, orange, and pink hues in seafood such as crabs, lobsters, shrimps, and pink salmon. Microalgae derived astaxanthin caters mostly to a niche market for natural pigments. Most of the marketed astaxanthin is made by synthetic chemical processes.

Chlorella, Arthrospira, Dunaliella, and H. pluvialis are the few species that are grown on large scale. Numerous other microalgae are grown as aquaculture feeds (Section 3.3), but on a much smaller scale compared to the above noted species. Of the above noted species, Chlorella, Arthrospira, and Dunaliella are typically grown outdoors in shallow ponds (20–30  cm deep) open to atmosphere. Circular or oblong ponds are typically used. Open culture systems tend to be cheap and this explains their use. No attempt is made to control contamination, but contamination is generally not a major issue as the few algal species grown commercially resist contamination either by virtue of rapid growth (Chlorella, one of the fastest growing microalgae) or extremophilic growth requirements, for example, alkaline pH for Arthrospira and hypersaline conditions for Dunaliella, that are poorly suited to potential contaminants. Extremophilic conditions are not used with H. pluvialis and, therefore, the green stage of this alga is typically grown in closed photobioreactors that minimize contamination. Once the green biomass has been produced, it is placed in outdoor open ponds to develop into astaxanthin-containing red hematocysts (aplanospores) under bright sunlight. In contrast to the above mentioned algae, most aquaculture feed algae are grown indoors at a relatively small scale under conditions that minimize contamination. This is because the optimal growth condition for many of these algae are such as to allow other potential contaminating algae to thrive.

The cyanobacterium Arthrospira (Spirulina) has been used as food by indigenous peoples of Asia, Africa, and the Americas for more than 1000  years. The Aztecs and other peoples of central Mexico harvested Arthrospira known to them as tecuitlatl, or tequitlatal, from local lakes for food. Fine nets were used to gather the biomass until around the 16th century. The consumption continued for nearly a 100  years after the Spanish conquest.

In Chad in West Africa, Arthrospira grows naturally in brackish alkaline water pools that form along the sandy northeastern shores of Lake Chad (Batello et al., 2004). Scooped pool water is drained through cloth to thicken the biomass slurry. In traditional processing, the thickened slurry is poured onto a circular patch of sand which absorbs the water. After about 20  min, the thin moist cake stuck on sand is cut into squares, peeled off and further dried. This thin sundried Arthrospira cake, or dihé, is sold in local markets (Batello et al., 2004). Dihé is made year round by indigenous women of the Kanembu people. Dihé is consumed mostly as a sauce. The dry cake is crumbled or ground, mixed with water, and cooked. Other ingredients may be added. The sauce is eaten with a stiff dough made of cooked ground sorghum or millet. More than 250 metric tons of dry Arthrospira is consumed annually as dihé (Batello et al., 2004). Globally, estimated commercial production of Arthrospira biomass is around 2000 dry tons. Production in the Kanem region of Chad therefore represents more than 10% of the global production. Modern commercial production of Arthrospira and its nutritional aspects are well documented in the literature (Gershwin and Belay, 2008). Large amounts of Arthrospira are produced in the United States and China.

3.3. Microalgae and Aquaculture

All wild caught seafood is a consequence of microalgae and cyanobacteria, the primary producers in most aquatic environments. Global annual per capita consumption of fish has increased from 9  kg in 1961 to nearly 20  kg today. Per capita consumption of other seafood (including freshwater species) has also increased. Global fisheries are overexploited and wild catch of fish appears to have peaked (Fig. 2.2).

Nearly 75% of the global fish catch is used for human consumption. The rest is converted to fish-meal and oil for feeding farmed fish and other animals. China is the world’s biggest consumer of seafood, followed by Japan and the United States. In some regions, fish is a major source of protein. Other countries with a high annual capita fish consumption are Iceland, Portugal, South Korea, Malaysia, Myanmar, Norway, and Spain. The top 10 most consumed seafoods in the United States are (in descending order of consumption): shrimps, canned tuna, salmon, tilapia, Alaska pollack, catfish, crab, cod, pangasius (a white fish), and clams. Consumption of these together is nearly 6  kg per capita annually in the United States.

Aquaculture is the farmed production of seafood. Aquaculture is relatively recent, although fish farming was practiced in ancient Egypt, China, Hawaii, India, Mesopotamia, and many other regions. In China evidence of fish farming goes back to nearly 3500  years. As wild caught seafood production cannot be increased sustainably (Jackson, 2012), aquaculture now supplies nearly 50% of the seafood consumed (Fig. 2.2). Demand for aquacultured products is growing. Production of farmed fish now tops world beef production. Global annual aquacultured seafood production is worth nearly US$100  billion. This excludes macroalgae (see Section 3.1). China is the largest producer of aquacultured seafood.

In principle, aquaculture is an efficient way of producing food. Fish typically convert more of the feed into body mass compared to terrestrial animals. For example, the feed conversion ratio of salmon is 1.2 (i.e., 1.2  kg of feed is consumed for each kg of biomass accumulated). In comparison, feed conversion ratios of beef, pork, and chicken are 8.7, 5.9, and 1.9, respectively. Unfortunately, aquaculture depends substantially on the marine wild catch. Aquaculture requires suitable feed including fishmeal and oil. Nearly 75% of the fishmeal is derived from whole marine fish for which the market is limited (e.g., sardines, anchovy, menhaden, sand eels and the unwanted bycatch of trawlers) (Jackson, 2012). The remaining 25% comes from by-products of fish processing for human consumption (Jackson, 2012). Increasing production of fishmeal and oil from wild catch is not sustainable. As microalgae are the basis of the marine food chain, in principle they can become the basis of food production by aquaculture. Crop plants provide some of the nutrients used in aquaculture feeds, but they cannot totally replace fishmeal and oil. This is because crop plants are deficient in some of the essential nutrients provided by fishmeal and oil. For example, plant proteins provide less amino acids such as lysine, methionine, threonine, and tryptophan (Henry, 2012). Many microalgae contain high levels of all essential amino acids (Henry, 2012). Other essential nutrients that microalgae can provide, but are lacking in terrestrial plants, include the nonprotein sulfonic acid taurine that is required by many carnivorous fish (Henry, 2012). Furthermore, microalgae can provide all the important long-chain polyunsaturated fatty acids (PUFA) found in fish oil. These fatty acids are essential to the health of marine animals.

Figure 2.2  Annual global food fish utilization from wild catch and aquaculture. 

Source: FAO, 2016. FAO Yearbook 2014: Fishery and Aquaculture Statistics. Food and Agriculture Organization of the United Nations, Rome.

Oils of coldwater fish are especially rich in polyunsaturated fatty acids such as EPA (eicosapentaenoic acid, C20:5n3, C20H30O2, an omega-3 fatty acid), DHA, and AA. Fish require these oils in their diet. In nature, they are derived via consumption of microalgae and bioaccumulation through the food chain. Microalgal biomass is rich in the requisite fatty acids, mainly long-chain polyunsaturated fatty acids, and can potentially replace fish oil and meal as a source of these fatty acids (Henry, 2012). Some marine species (e.g., lobsters, crabs, shrimps, salmon, red snapper, red mullet) require microalgae-sourced bioaccumulated pigments such as astaxanthin that can be obtained via cultured microalgae. In principle, processed microalgal biomass can replace fishmeal and oil as aquaculture feeds (Sarker et al., 2016), so long as it is produced in sufficient quantity and cheaply.

Not all microalgae are suitable aquaculture feeds (Wikfors and Ohno, 2001). A suitable feed alga must have the essential nutrients (e.g., the required fatty acids, sterols, pigments, etc.) and it must be ingestible and digestible by the relevant aquatic animals. In addition, it must be free of potentially toxic substances. Microalgae commonly used as aquaculture feeds include strains of Isochrysis, Pavlova, Nannochloropsis, Tetraselmis, Thalassiosira, and Chaetoceros (Wikfors and Ohno, 2001).

Filter-feeding mollusks such as oysters, clams, and scallops require microalgae feeds throughout life (Wikfors and Ohno, 2001). The larval stages of these shellfish are initially fed on aquacultured microalgae and then planted in the sea to thrive on wild algae. Larval shrimps may be fed directly with microalgae, but soon require a diet of live feeds consisting of zooplankton (rotifers and copepods). Larval stages of finfish are fed on live feeds and later with pelleted feed.

Rotifers for feed are commonly grown using microalgae and other microbial feeds. Irrespective of the feed used, just prior to being fed to larval fish, rotifers are typically conditioned on algal feeds (Wikfors and Ohno, 2001). This fills up their guts with algae to provide nutrients from partially digested algae to the fish (Wikfors and Ohno, 2001). The salt water rotifers commonly used as feeds are the large-sized Brachionus plicatilis (60–350  μm in length) and the smaller B. rotundiformis (120–180  μm in length). Later stage larval fish may be fed brine shrimp (Artemia salina; 400–800  μm in length) and various Daphnia species (0.2–5  mm in length).

Pelleted feed for finfish contains nutrients from plant sources (e.g., soyprotein), fishmeal, and fish oil. Fishmeal and oil are generally necessary components. Feed pellets for carnivorous fish species may contain

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