Cellular Differentiation in the Cyanobacterium Nostoc Punctiforme

Arch Microbiol (2002) 178:395–403 DOI 10.1007/s00203-002-0476-5 MINI-REVIEW John C. Meeks · Elsie L. Campbell · Michael L. Summers · Francis C. Wong Cellular differentiation in the cyanobacterium Nostoc punctiforme Received: 14 May 2002 / Revised: 25 July 2002 / Accepted: 12 August 2002 / Published online: 18 September 2002 © Springer-Verlag 2002 Abstract Nostoc punctiforme is a phenotypically complex, filamentous, nitrogen-fixing cyanobacterium, whose Introduction vegetative cells can mature in four developmental directions. The particular developmental direction is deter- Nostoc punctiforme [Pasteur Culture Collection (PCC) mined by environmental signals. The vegetative cell cycle 73102, synonym American Type Culture Collection (ATCC) is maintained when nutrients are sufficient. Limitation for 29133] is a filamentous nitrogen-fixing cyanobacterium combined nitrogen induces the terminal differentiation of with an extraordinarily wide range of ecological niches, heterocysts, cells specialized for nitrogen fixation in an physiological properties and vegetative cell developmen- oxic environment. A number of unique regulatory events tal alternatives. The developmental biology of N. puncti- and genes have been identified and integrated into a work- forme is the topic of this review. The shotgun phase of se- ing model of heterocyst differentiation. Phosphate limita- quencing the N. punctiforme genome has been completed tion induces the transient differentiation of akinetes, (http://www.jgi.doe.gov) and a preliminary analysis was spore-like cells resistant to cold and desiccation. A variety recently published (Meeks et al. 2001). N. punctiforme is of environmental changes, both positive and negative for amenable to genetic manipulations (Cohen et al. 1994), growth, induce the transient differentiation of hormogo- including targeted gene replacement (Campbell et al. nia, motile filaments that function in dispersal. Initiation 1998). The combination of genome sequence information, of the differentiation of heterocysts, akinetes and hor- genetic tractability and expression of multiple phenotypic mogonia are hypothesized to depart from the vegetative traits makes N. punctiforme ideal for detailed molecular cell cycle, following separate and distinct events. N. punc- characterization of a bacterium with a complex life cycle. tiforme also forms nitrogen-fixing symbiotic associations; Vegetative cells of N. punctiforme can mature in four its plant partners influence the differentiation and behav- developmental directions (Figs.1, 2). First, the cells can ior of hormogonia and heterocysts. N. punctiforme is ge- successively grow and divide to perpetuate the vegetative netically tractable and its genome sequence is nearly com- cell cycle when nutrients are unlimited (Figs.1, 2A). Of plete. Thus, the regulatory circuits of three cellular differ- the three vegetative cell developmental alternatives, the entiation events and symbiotic interactions of N. puncti- differentiation of N2-fixing heterocysts in the absence of forme can be experimentally analyzed by functional ge- combined nitrogen is the most highly studied develop- nomics. mental event in cyanobacteria and is commonly recog- nized as a taxonomic trait (Fig.2B). Nitrogenase, the en- + Keywords Akinetes · Cellular differentiation · zyme catalyzing N2 reduction to NH4 is oxygen-sensitive Cyanobacteria · Heterocysts · Hormogonia · Nostoc (Wolk et al. 1994). Therefore, N2 fixation appears incom- punctiforme · Symbiosis patible with oxygenic photosynthesis, the unifying physiological characteristic of cyanobacteria. Highly specialized, terminally differentiated, microoxic heterocysts are the evolutionary solution to the incompatibility dilemma J.C. Meeks (✉) · E.L. Campbell · F.C. Wong in all filamentous cyanobacteria in the orders Nostocales Section of Microbiology, University of California, Davis, CA 95616, USA and Stigonemateles (Castenholz and Waterbury 1989). In e-mail: [email protected], the second developmental alternative, some or all vegeta- Tel.: 1-530-7523346, Fax: 1-530-7529014 tive cells of N. punctiforme can transiently differentiate into M.L. Summers spore-like structures (Fig.2C), called akinetes in cyano- Department of Biology, California State University, bacteria (Castenholz and Waterbury 1989). Akinetes are Northridge, CA 91330-8303, USA more resistant than vegetative cells to cold and desicca- 396 Fig.1 Schematic of the Nostoc punctiforme vegetative cell cycle lates. A schematic of the hypothetical N. punctiforme veg- and points where specific developmental events are hypothesized etative cell cycle and the postulated relationship of the to depart from the cell cycle. N. punctiforme does not form branch- ing filaments; thus, its life cycle of polar vegetative cell growth, three developmental alternatives to cell cycle events are DNA replication and chromosome segregation, followed by cell depicted in Fig.1. The schematic is based more on deduc- division in a transverse plane, is modeled as similar to unicellular tive reasoning than experimental fact and is presented as a bacteria. Physiological processes are denoted adjacent to the cell working model. cycle or developmental event. In general, cyanobacteria have mul- The four developmental directions of a N. punctiforme tiple copies of the chromosome per cell. Only four copies are depicted here, but N. punctiforme is likely to have more than four. vegetative cell are numerically unparalleled in the pro- The hypothesized developmental departure points leading to a de- karyotic world. Other bacteria have at most two or three velopmental destination are represented by dashed lines; and developmental choices, such as those that can sporulate phrases in parentheses represent the environmental signal initiat- and/or form motile swarmer or gliding cells, along with ing the developmental event. Heterocyst differentiation requires DNA replication after cell division, but akinetes appear to have the vegetatively competent prosthecate or undifferentiated same DNA content as vegetative cells. Therefore, akinetes are de- cells, or subsurface and aerial mycelia and spores (Kaiser picted as departing from the cycle after cell division and prior to and Losick 1993; Roberts et al. 1996). Moreover, hetero- DNA replication, while heterocysts are depicted as departing at an cyst, akinete and hormogonium differentiation occur only unknown point during DNA replication (the unrooted dashed line). Hormogonium differentiation involves cell division uncou- following signals of a specific environmental change, in pled from DNA replication and, therefore, the departure of hor- contrast to the obligatory formation of swarmer cells by mogonia coincides with septal ring formation and cell division prosthecate bacteria (Roberts et al. 1996). Therefore, all three developmental alternatives can be eliminated by mutation and the N. punctiforme mutants maintained for tion (Adams and Duggan 1999). Akinete differentiation is analysis under the permissive growth conditions. How the confined to the heterocyst-forming cyanobacteria. The environmental signals are perceived, integrated and elicit third developmental alternative is the transient differenti- three distinct differentiation events is of fundamental bio- ation of vegetative filaments into motile filaments called logical interest. hormogonia (Fig.2D). Hormogonium filaments lack hete- An objective of this review is to briefly summarize rocysts, do not fix N2 and function in short-distance dis- knowledge of cellular differentiation resulting from analy- persal (Tandeau de Marsac 1994). Some, but not all, hete- ses of N. punctiforme and related cyanobacteria, such as rocyst-forming and heterocyst-non-forming filamentous Anabaena sp. strain PCC 7120, with which genetic proto- cyanobacteria can differentiate hormogonia (Castenholz cols for filamentous cyanobacteria were developed (Thiel and Waterbury 1989). Specifically, hormogonium differ- 1994). Anabaena sp. strain PCC 7120 has received the entiation has been used to distinguish the morphologically most attention as an experimental system for analysis of similar genera Nostoc (positive) and Anabaena (negative; heterocyst differentiation (Golden and Yoon 1998; Adams Rippka et al. 1979). The fact that differentiation of motile 2000; Wolk 2000). Anabaena sp. strain PCC 7120 is hormogonia is often lost in culture minimizes its taxo- genotypically a Nostoc species (Rippka and Herdman nomic application, except in feral samples or recent iso- 1992) that, presumably due to mutation during prolonged 397 In most studies of developmentally competent cyanobacteria, the experimental focus has been on responses of axenic cultures (Tandeau de Marsac 1994; Wolk et al. 1994; Adams and Duggan 1999). N. punctiforme forms symbiotic associations with specific representatives of the major phylogenetic groups of spore- and seed-producing plants, including bryophyte hornworts (Meeks 1998), gymnosperm cycads (source for isolation; Rippka et al. 1979) and the angiosperm Gunnera (Rai et al. 2000). Sym- biotic associations, such as that with the hornwort Antho- ceros punctatus, are of interest because the plant partner influences the differentiation of hormogonia (Campbell and Meeks 1989; Cohen and Meeks 1997) and heterocysts (Meeks and Elhai 2002); the symbiotic Nostoc shifts to a largely heterotrophic metabolic mode (Meeks 1998). Heterocyst differentiation Physiologically, heterocysts may be considered as sinks of reduced carbon and sources of reduced nitrogen

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