Heterotrophy among Cyanobacteria

Abstract

Cyanobacteria have been studied in recent decades to investigate the principle mechanisms of plant-type oxygenic photosynthesis, as they are the inventors of this process, and their cultivation and research is much easier compared to land plants. Nevertheless, many cyanobacterial strains possess the capacity for at least some forms of heterotrophic growth. This review demonstrates that cyanobacteria are much more than simple photoautotrophs, and their flexibility toward different environmental conditions has been underestimated in the past. It summarizes the strains capable of heterotrophy known by date structured by their phylogeny and lists the possible substrates for heterotrophy for each of them in a table in the Supporting Information. The conditions are discussed in detail that cause heterotrophic growth for each strain in order to allow for reproduction of the results. The review explains the importance of this knowledge for the use of new methods of cyanobacterial cultivation, which may be advantageous under certain conditions. It seeks to stimulate other researchers to identify new strains capable of heterotrophy that have not been known so far.

Figure 1

Overview of uptake and metabolization of diverse organic molecules by a cyanobacterial cell. GlpK, glycerol kinase; XylA, xylose isomerase; XylB, xylulokinase; Glk, glucokinase; CscA/InvA, invertase; CscK, fructokinase (from E. coli). The “?” at the glycerol transporter implies that this transporter and the corresponding gene in Cyanothece sp. ATCC 51142 have not been identified yet. The “?” after the (native cyanobacterial) fructokinase indicates that no gene within the genome of either Anabaena sp. ATCC 29413 or Nostoc sp. ATCC 29133 has been annotated as fructokinase so far.

Figure 2

Growth (A) and glucose uptake (B) of Synechococcus PCC7942 WT and R2–1 cells incubated under the indicated trophic conditions. All cultures of R2–1 contained streptomycin. A: WT, photoautotrophy (▲); R2–1, photoautotrophy (□), transferred from photoautotrophy to photoheterotrophy (■, lower line), maintained under photoheterotrophy (■, upper line). B: WT (▲); R2–1 pregrown under photoautotrophy (□), adapted to photoheterotrophy (■). WT Synechocystis PCC6803 grown under photoautotrophy (+). The growth curves shown represent one typical set of 3–4 repeats. Reprinted with permission from ref (39). Copyright 1998 Oxford University Press.

Figure 3

Installation of the glucose transporter to S. elongatus. (A) Schematic representation of the glucose transporter gene integration into the S. elongatus genome. (B) Growth curve of the galP strain (red) and wild type (blue) with and without 5 g/L glucose. (C) Growth curve of the Glut1 (purple) and glcP (green) strains and the wild type. (D) Growth curve of the galP strain and the wild type with and without glgC deletion (glgC KO). For panels B, C, and D, empty symbols are samples in BG-11 medium without glucose, while solid symbols indicate results with BG-11 containing 5 g/L glucose. White and shaded areas indicate the light and dark cycles, respectively. All y axes denote OD₇₃₀, although the scales differ for visibility. Error bars represent standard deviations (in triplicate). NSI, neutral site 1. Reprinted with permission from ref (60). Copyright 2013 American Society for Microbiology.

Figure 4

Installation of the sucrose degradation pathway. (A) Schematic representation of integration of the sucrose degradation pathway into the S. elongatus chromosome. (B) Synthetic sucrose degradation pathway in S. elongatus. Red arrows indicate steps catalyzed by heterologous enzymes. PPP, pentose phosphate pathway. (C) Growth curves of the cscB–cscK strain (red) and the wild type (blue). Empty and filled symbols indicate growth without and with 5 g/L sucrose, respectively. White and shaded areas indicate light and dark cycles, respectively. Error bars represent standard deviations (in triplicate). Reprinted with permission from ref (60). Copyright 2013 American Society for Microbiology.

Figure 5

Installation of the xylose degradation pathway. (A) Schematic representation of integration of the xylose degradation pathway into the S. elongatus chromosome. (B) Synthetic xylose degradation pathway in S. elongatus. Red arrows indicate steps catalyzed by heterologous enzymes. (C) Growth curves of the xylE and xylEAB strains and wild type. Empty and filled symbols indicate growth without and with 5 g/L xylose, respectively. White and shaded areas indicate light and dark cycles. Error bars represent standard deviations (in triplicate). Reprinted with permission from ref (60). Copyright 2013 American Society for Microbiology.

Figure 6

Photomixotrophic (A) and photoheterotrophic (B) growths of Synechocystis sp. PCC 6803 gtr^– dependent on (blue diamond) 0 mM, (red square) 50 mM, (green triangle) 100 mM, and (×) 200 mM fructose. Reprinted with permission from the authors of ref (74).