The Choanoflagellates: Evolution, Biology and Ecology

Most of life on earth is microscopic and unicellular. Unicellular eukaryotes are specifically important as they comprise a tremendous diversity and are an important link in carbon and element cycling. In marine food webs heterotrophic protists, specifically heterotrophic nanoflagellates, channel carbon and element transfer from bacterial production to higher trophic levels. Among these the choanoflagellates deserve closer attention, specifically in the context of ecology and evolutionary biology. Choanoflagellates are important consumers of bacteria. Being unicellular filter feeders, choanoflagellates are important bacterivores in aquatic environments, both in marine and freshwater. Beyond their ecological importance they are important in evolutionary biology as the closest unicellular relatives of Metazoa.

Since the first description of choanoflagellates in 1866 by James-Clark, knowledge about the biology of these organisms has accumulated in the scientific literature. With the present book, the world authority on chonaoflagellate research, Barry Leadbeater, summarizes the current knowledge on these ecologically and evolutionarily important and often overlooked organisms. As the author states in the foreword, ‘time has come to consolidate an extensive body of literature into book format’. The ambitious aim of this book is to provide a comprehensive overview on the current knowledge of all aspects of choanoflagellate biology.

One main theme permeates the volume: the construction of the organic thecae and siliceous loricae in choanoflagellates, the ultrastructure of the assembly of these structures and their evolutionary significance. Consequently, the sections on lorica construction and assembly are more detailed than the other sections.

The book is structured into 10 chapters with the first two chapters providing a general overview on choanoflagellate research and functional morphology, Chapters 3–8 focusing specifically on the morphology and ultrastructure of choanoflagellate thecae and loricae, and Chapters 9–10 placing this knowledge in an ecological (Chapter 9) and evolutionary (Chapter 10) context.

The first chapter provides a historical overview of choanoflagellate research, specifically focusing on the discovery of choanoflagellates and the contributions of early investigators. Considerable attention is given to the historic importance of choanoflagellate research for the development of concepts of the early evolution of the Metazoa. The morphological similarity of the choanocyte of sponges and choanoflagellate cells stimulated ideas on the evolution and phylogenetic position of sponges as well as concepts of early metazoan evolution, such as Haeckel's gastraea theory.

Due to the small size of choanoflagellates, and of protists in general, aquatic life is somewhat different from that of larger organisms. For small organisms water is quite viscous, a phenomenon referred to as life at low Reynolds numbers. Swimming as well as prey capture is therefore special. The lorica of choanoflagellates further modifies hydrodynamics and water currents. These aspects are the focus of the second chapter that deals with the functional morphology of choanoflagellates. Movement and prey capture are central, but this chapter also covers form and function of cell organelles and the nucleus.

Molecular data in concert with ultrastructural data are currently changing our perception of choanoflagellate phylogeny and systematics: whereas the order Craspedida comprises exclusively species with organic coverings, the order Acanthoecida contains taxa with siliceous loricae. Chapters 3–8 deal with more specific aspects of these two choanoflagellate orders, specifically the importance of the lorica as a morphological feature both for understanding the evolutionary relationships among choanoflagellates as well as for aspects of ecology and general biology. Consequently, a main focus of these chapters lies on the extracellular coverings, i.e. the organic theca of the Craspedida and the siliceous lorica of the Acanthoecida. Chapter 3 concludes with aspects of encystment in the Craspedida and a discussion on the phylogenetic value of microfibril polymerization.

Chapters 4–8 focus on the order Acanthoecida and deal with the general lorica construction. Chapter 4 begins with a brief introduction into the Acanthoecida including a detailed terminology of choanoflagellate loricae and technical aspects of lorica preservation for electron microscopical investigations, and concludes with general rules for lorica construction and assembly.

Silicon availability plays a crucial role in lorica construction. This aspect is extensively discussed in Chapter 5. Starting with some general aspects of silicon cycling in seawater, silicon turnover is discussed extensively for the model species Stephanoeca diplocostata W.N. Ellis, 1930. The ultrastructure of strip production forms another large part of this chapter emphasizing specifically the role of microtubules and silicon availability. The chapter closes with a discussion placing this aspect in a broader context.

Chapter 6 deals with lorica construction in nudiform taxa, i.e. in the Acanthoecida. After a general introduction the details of lorica construction and assembly are outlined for each of the four nudiform genera. Again, the role of microtubules is highlighted. The chapter concludes with a discussion-like paragraph on the monophyly of nudiform choanoflagellates.

Chapter 7 deals with tectiform taxa that are grouped within the family Stephanoecida – a monophyletic lineage being either sister to the nudiform taxa or branching within the latter, making the nudiform taxon paraphyletic. This chapter focusses on lorica construction and assembly of the up-to-date best investigated species S. diplocostata, Didymoeca costata (Valkanov) Dowdwell, 2003 and Diaphanoeca grandis Ellis, 1930.

The evolutionary implications of lorica morphology and assembly, which have been extensively described in the foregoing chapters, are discussed in Chapter 8.

The ecology of choanoflagellates is dealt with in Chapter 9. Starting with a brief introduction into the general ecology of heterotrophic nanoflagellates, this chapter concentrates on aspects of osmotrophic nutrition and phagotrophic nutrition as well as on the growth kinetics of choanoflagellates as a function of bacterial food concentration. These aspects of choanoflagellate feeding ecology are followed by an extensive overview of the ecology and distribution of choanoflagellates in the marine environment and a comparatively short section on freshwater and soil choanoflagellates.

Chapter 10 again deals with evolutionary aspects, now highlighting ophistokont evolution and systematics as well as early metazoan evolution. In this context, other early branching taxa such as the Ichthyosporea, Filasterea and Corallochytrea are also considered. The evolution of metazoan multicellularity and related aspects such as cell–cell adhesion and signaling are central to this chapter.

A significant strength of the book is its comprehensive approach to all aspects of choanoflagellate biology combined with the author's extensive experience with this group. The book therefore is an all-embracing state-of-the-art snapshot of choanoflagellate research. Incorporating the findings of recent research articles, many chapters have a format of scientific review articles concluding with a discussion of the different potential implications of the actual state of research rather than explicit concluding statements. The book is therefore a comprehensive overview on the current knowledge of choanoflagellate biology. A focus on systematics and morphological and evolutionary aspects reflects the past and current research in this field and of the author. Taken together, the author has managed to include all aspects of choanoflagellate biology into a single book. The illustrations are excellent throughout the book and the author managed to include the most recent scientific findings and lines of discussion. It is therefore a valuable book for anyone interested in the diversity of eukaryotes and the biology of heterotrophic nanoflagellates and a must for anyone addressing any aspect of choanoflagellate biology.