The Multicellular Nature of Filamentous Heterocyst-Forming Cyanobacteria Antonia Herrero1,∗,Joelstavans2 and Enrique Flores1 Downloaded From
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FEMS Microbiology Reviews, fuw029, 40, 2016, 831–854 doi: 10.1093/femsre/fuw029 Review Article REVIEW ARTICLE The multicellular nature of filamentous heterocyst-forming cyanobacteria Antonia Herrero1,∗,JoelStavans2 and Enrique Flores1 Downloaded from 1Instituto de Bioqu´ımica Vegetal y Fotos´ıntesis, CSIC and Universidad de Sevilla, Americo´ Vespucio 49, E-41092 Seville, Spain and 2Department of Physics of Complex Systems, Weizmann Institute of Science, Rehovot 76100, Israel ∗Corresponding author: Americo Vespucio s/n, Seville, 41092, Spain. Tel: +34-954460165; Fax: +34-954460165; E-mail: [email protected] http://femsre.oxfordjournals.org/ One sentence summary: The organismic unit in heterocyst-forming cyanobacteria is a filament of interconnected cells; to gain an understanding of multicellularity in these organisms, the authors analyze and discuss their filament structure, theoretical models of heterocyst pattern formation,and their distinct cell division characteristics. Editor: William Margolin ABSTRACT Cyanobacteria carry out oxygenic photosynthesis, play a key role in the cycling of carbon and nitrogen in the biosphere, and have had a large impact on the evolution of life and the Earth itself. Many cyanobacterial strains exhibit a multicellular by guest on November 25, 2016 lifestyle, growing as filaments that can be hundreds of cells long and endowed with intercellular communication. Furthermore, under depletion of combined nitrogen, filament growth requires the activity of two interdependent cell types: vegetative cells that fix 2CO and heterocysts that fix N2. Intercellular molecular transfer is essential for signaling involved in the regulation of heterocyst differentiation and for reciprocal nutrition of heterocysts and vegetative cells. Here we review various aspects of multicellularity in cyanobacterial filaments and their differentiation, including filament architecture with emphasis on the structures used for intercellular communication; we survey theoretical models that have been put forward to understand heterocyst patterning and discuss the factors that need to be considered for these models to reflect the biological entity; and finally, since cell division in filamentous cyanobacteria has the peculiarity of producing linked instead of independent cells, we review distinct aspects of cell division in these organisms. Keywords: Anabaena; cell differentiation; cyanobacteria; heterocysts; intercellular communication; multicellularity INTRODUCTION a high respiratory rate. Moreover, ancestral cyanobacteria gave rise by symbiosis to the plastids of all extant algae and plants. The emergence of oxygenic photosynthesis in cyanobacterial Thus, the evolution of eukaryotic organisms relied to a great de- ancestors at about 3 Gyr ago (Gya) was one of the major revolu- gree on ancient cyanobacteria (see Ku et al. 2015). Currently, plas- tions in the history of life on Earth. Cyanobacterial activity was tids, which perform cyanobacterial-like photosynthesis, and ex- responsible for the accumulation of oxygen in the atmosphere tant cyanobacteria, which inhabit almost all natural habitats, and surface waters that led to the Great Oxygenation Event (GEO) contributes most of the primary production that is at the basis 2.4–2.3 Gya, which started to change the Earth’s environment of the trophic chains in the biosphere. In addition, cyanobac- and challenged the existent forms of life to cope with, or in teria are dominant N2 fixers in the oceans, introducing assim- most cases to take advantage of, the available oxygen (see Lyons, ilable nitrogen into the biosphere. In view of their remarkable Reinhard and Planavsky 2014). This trend would eventually lead role, the title ‘The cyanobacteria, life’s microbial heroes’ given by to the development of oxygenic respiration and animals with Received: 10 May 2016; Accepted: 9 July 2016 C FEMS 2016. All rights reserved. For permissions, please e-mail: [email protected] 831 832 FEMS Microbiology Reviews, 2016, Vol. 40, No. 6 A. H. Knoll to a chapter of his book on the history of life on Earth of the trichome occurs mainly by intercalary cell division and appears to be most justified (Knoll 2004; see also Knoll 2008). that reproduce by random trichome breakage. In cyanobacte- Multicellularity can be defined as a form of biological organi- ria of Section III, the filaments are made of a single cell type zation in which a permanent cell aggregate exhibits an activity and cell division takes place in a plane perpendicular to the tri- more complex than that of the individual cells. Multicellularity chome’s long axis producing uniseriate filaments and hormogo- is a major evolutionary innovation that marks a new level of or- nia in some strains. Cyanobacteria of Sections IV and V have the ganization, together with a shift of the unit of selection from capacity for cell differentiation into heterocysts and, in many single cells to an organism (Szathmary and Smith 1995), and is but not all strains, into akinetes and/or hormogonia. Members a requisite for the development of adaptive complexity. Possible of Sections IV and V are distinguished by cell division. Whereas scenarios for the emergence of multicellular life forms include in Section IV cyanobacteria cell division takes place perpendic- cell clustering and cooperative behavior of unicellular organ- ular to the long axis of the filament, in Section V cyanobacte- isms, as well as the appearance of physical factors or mutations ria some divisions take place at a different angle, giving rise that may have prevented the separation of dividing cells (Bonner to filaments with true branches. Phylogenetic analysis based 1998). To survive, the selective advantages of an aggregated life on 16S rRNA sequences and concatenated protein sequences form must exceed likely shortcomings such as increased com- has led to the construction of evolutionary trees with extant petition for local resources, reduced mobility, and the presence species organized in a few clades, which have been compared of non-cooperator or cheater cells that reap the benefits of co- to Sections I–V based on morphology (Shih et al. 2013;Sanchez-´ operation but do not bear its costs, leading cooperators to ex- Baracaldo, Ridgwell and Raven 2014; Schirrmeister, Gugger and tinction and thus to the celebrated ‘tragedy of the commons’ Donoghue 2015). Among these five taxonomic units, only Sec- Downloaded from (Hardin 1968;Westet al. 2006). Although other aggregative forms tions IV and V jointly are monophyletic (Giovannoni et al. 1988; are found (e.g. in magnetotactic bacteria, see Abreu et al. 2013), a Shih et al. 2013; Schirrmeister, Gugger and Donoghue 2015). Mul- simple form of multicellular organization is found when an or- ticellular cyanobacteria are identified with filamentous strains, ganism grows as chains of cells. Bacteria that grow taking the especially those capable of cell differentiation, which constitute form of filaments can be found in different phylogenetic groups. the main subject of this review. However, although traditionally To give just a few examples, other than the cyanobacteria, the considered unicellular, some representatives of Section I form http://femsre.oxfordjournals.org/ Actinobacteria (Flardh¨ and Buttner 2009), Desulfobulbaceae (Pfef- characteristic cell aggregates enclosed in laminar sheaths, and fer et al. 2012)andLachnospiraceae (Thompson et al. 2012)contain some representatives of Section II form aggregates of firmly ad- filamentous forms, and bacteria of the genera Chloroflexus (Pier- hered vegetative cells enclosed by an additional fibrous layer son and Castenholz 1974), Beggiatoa (Strohl and Larkin 1978)and (Rippka et al. 1979). It would be worth investigating whether Entotheonella (Wilson et al. 2014) are filamentous. The structure these cell aggregates exhibit some social characteristics of of such filaments can, however, be very different. Thus, whereas multicellularity. Streptomyces forms hyphae, the filamentous cyanobacteria form chains of cells. FILAMENTOUS CYANOBACTERIA Extant cyanobacteria present a large morphological diversity comprising unicellular forms and filaments with different de- Filamentous cyanobacteria are among the oldest multicellular by guest on November 25, 2016 grees of complexity, including uniseriate and multiseriate or- organisms on our planet. The cyanobacteria constitute a mono- ganizations and three recognized developmental alternatives. phyletic group and, although the last universal ancestor of the Cell differentiation in filamentous cyanobacteria includes that cyanobacterial phylum was most likely unicellular, both 16S of micro-oxic cells, called heterocysts, specialized in the fix- rRNA and genome-scale phylogenetic analyses support an an- ation of atmospheric nitrogen (N2), which takes place under cient occurrence of multicellular cyanobacteria, already present conditions of nitrogen deprivation and allows performance of by the end of the Archean eon before the GOE (Schirrmeister, An- the extremely O2-sensitive N2-fixation machinery in oxic envi- tonelli and Bagheri 2011; Schirrmeister et al. 2013; Schirrmeister, ronments; of resting cells called akinetes; and of short repro- Gugger and Donoghue 2015;Shihet al. 2013). Indeed, multicel- ductive filaments made of small cells called hormogonia (Flo- lularity could have led to increased metabolic performance fa- res and Herrero 2014). Additionally, necridia resulting from pro- voring diversification and extension of cyanobacteria in Nature, grammed