Growth of the Cyanobacterium Synechococcus leopoliensis CCAP1405/1 on Agar Media in the Presence of Heterotrophic Bacteria

Hayashi, Shinobu; Itoh, Kazuhito; Suyama, Kousuke

doi:10.1264/jsme2.me10193

Cited by 16 publications

(19 citation statements)

References 38 publications

(43 reference statements)

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“…This increase indicates that the eukaryotic heterotroph may provide additional benefits to phototrophic partners in addition to HOOH elimination in order to support the growth of cyanobacteria even more. Previous studies have shown that the addition of thiosulfate, vitamin B12, biotin, and thiamine can be used to enhance and elevate the growth of the cyanobacterium Synechococcus leopoliensis CCAP1405/1 [44]. …”

Section: Resultsmentioning

confidence: 99%

Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform

Butler

et al. 2017

Biotechnol Biofuels

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BackgroundThe feasibility of heterotrophic–phototrophic symbioses was tested via pairing of yeast strains Cryptococcus curvatus, Rhodotorula glutinis, or Saccharomyces cerevisiae with a sucrose-secreting cyanobacterium Synechococcus elongatus.ResultsThe phototroph S. elongatus showed no growth in standard BG-11 medium with yeast extract, but grew well in BG-11 medium alone or supplemented with yeast nitrogen base without amino acids (YNB w/o aa). Among three yeast species, C. curvatus and R. glutinis adapted well to the BG-11 medium supplemented with YNB w/o aa, sucrose, and various concentrations of NaCl needed to maintain sucrose secretion from S. elongatus, while growth of S. cerevisiae was highly dependent on sucrose levels. R. glutinis and C. curvatus grew efficiently and utilized sucrose produced by the partner in co-culture. Co-cultures of S. elongatus and R. glutinis were sustained over 1 month in both batch and in semi-continuous culture, with the final biomass and overall lipid yields in the batch co-culture 40 to 60% higher compared to batch mono-cultures of S. elongatus. The co-cultures showed enhanced levels of palmitoleic and linoleic acids. Furthermore, cyanobacterial growth in co-culture with R. glutinis was significantly superior to axenic growth, as S. elongatus was unable to grow in the absence of the yeast partner when cultivated at lower densities in liquid medium. Accumulated reactive oxygen species was observed to severely inhibit axenic growth of cyanobacteria, which was efficiently alleviated through catalase supply and even more effectively with co-cultures of R. glutinis.ConclusionsThe pairing of a cyanobacterium and eukaryotic heterotroph in the artificial lichen of this study demonstrates the importance of mutual interactions between phototrophs and heterotrophs, e.g., phototrophs provide a carbon source to heterotrophs, and heterotrophs assist phototrophic growth and survival by removing/eliminating oxidative stress. Our results establish a potential stable production platform that combines the metabolic capability of photoautotrophs to capture inorganic carbon with the channeling of the resulting organic carbon directly to a robust heterotroph partner for producing biofuel and other chemical precursors.Electronic supplementary materialThe online version of this article (doi:10.1186/s13068-017-0736-x) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform

Butler

et al. 2017

Biotechnol Biofuels

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“…WH2K promotes specific adherence of the epibionts to the cyanobacterial heterocysts (Stevenson and Waterbury, 2006; Behrens et al, 2008; Stevenson et al, 2011). Many cyanobacteria grow more efficiently in co-cultivation with heterotrophic bacteria than in axenic cultures, especially when heterotrophic remineralization of organic carbon alleviates cyanobacterial carbon limitation (Lupton and Marshall, 1981; Schiefer and Caldwell, 1982; Morris et al, 2008; Abed, 2010; Hayashi et al, 2011; Shen et al, 2011). Specific, highly-adapted interspecies interactions improve nutrient (Paerl, 1977; Paerl and Kellar, 1978; Lupton and Marshall, 1981; Li et al, 2010; Roe et al, 2012; Van Mooy et al, 2012) and vitamin (Gordon et al, 1969; Kazamia et al, 2012; Xie et al, 2013) acquisition by cyanobacteria and eukaryotic microalgae in consortia.…”

Section: Introductionmentioning

confidence: 99%

Phototrophic biofilm assembly in microbial-mat-derived unicyanobacterial consortia: model systems for the study of autotroph-heterotroph interactions

et al. 2014

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Microbial autotroph-heterotroph interactions influence biogeochemical cycles on a global scale, but the diversity and complexity of natural systems and their intractability to in situ manipulation make it challenging to elucidate the principles governing these interactions. The study of assembling phototrophic biofilm communities provides a robust means to identify such interactions and evaluate their contributions to the recruitment and maintenance of phylogenetic and functional diversity over time. To examine primary succession in phototrophic communities, we isolated two unicyanobacterial consortia from the microbial mat in Hot Lake, Washington, characterizing the membership and metabolic function of each consortium. We then analyzed the spatial structures and quantified the community compositions of their assembling biofilms. The consortia retained the same suite of heterotrophic species, identified as abundant members of the mat and assigned to Alphaproteobacteria, Gammaproteobacteria, and Bacteroidetes. Autotroph growth rates dominated early in assembly, yielding to increasing heterotroph growth rates late in succession. The two consortia exhibited similar assembly patterns, with increasing relative abundances of members from Bacteroidetes and Alphaproteobacteria concurrent with decreasing relative abundances of those from Gammaproteobacteria. Despite these similarities at higher taxonomic levels, the relative abundances of individual heterotrophic species were substantially different in the developing consortial biofilms. This suggests that, although similar niches are created by the cyanobacterial metabolisms, the resulting webs of autotroph-heterotroph and heterotroph-heterotroph interactions are specific to each primary producer. The relative simplicity and tractability of the Hot Lake unicyanobacterial consortia make them useful model systems for deciphering interspecies interactions and assembly principles relevant to natural microbial communities.

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“…The spectrum of behavioral responses varies greatly, as the origin of excreted material ranges from targeted secretion of photosynthetic intermediates (for example, glycolate, osmolytes and fatty acids) and extracellular polymeric substance (Seymour et al, 2010;Bruckner et al, 2011), to the products of cell lysis that can include sugars, proteins, lipids and nucleic acids (Grossart, 1999;Stevenson and Waterbury, 2006;Shen et al, 2011). In exchange, heterotrophic bacteria are thought to provide essential micronutrients, such as vitamins, amino acids and bioavailable trace metals (Amin et al, 2009;Hayashi et al, 2011;Kazamia et al, 2012;Xie et al, 2013), necessary to maintain high photosynthetic productivity.…”

Section: Introductionmentioning

confidence: 99%

Inference of interactions in cyanobacterial–heterotrophic co-cultures via transcriptome sequencing

et al. 2014

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We used deep sequencing technology to identify transcriptional adaptation of the euryhaline unicellular cyanobacterium Synechococcus sp. PCC 7002 and the marine facultative aerobe Shewanella putrefaciens W3-18-1 to growth in a co-culture and infer the effect of carbon flux distributions on photoautotroph-heterotroph interactions. The overall transcriptome response of both organisms to co-cultivation was shaped by their respective physiologies and growth constraints. Carbon limitation resulted in the expansion of metabolic capacities, which was manifested through the transcriptional upregulation of transport and catabolic pathways. Although growth coupling occurred via lactate oxidation or secretion of photosynthetically fixed carbon, there was evidence of specific metabolic interactions between the two organisms. These hypothesized interactions were inferred from the excretion of specific amino acids (for example, alanine and methionine) by the cyanobacterium, which correlated with the downregulation of the corresponding biosynthetic machinery in Shewanella W3-18-1. In addition, the broad and consistent decrease of mRNA levels for many Fe-regulated Synechococcus 7002 genes during co-cultivation may indicate increased Fe availability as well as more facile and energy-efficient mechanisms for Fe acquisition by the cyanobacterium. Furthermore, evidence pointed at potentially novel interactions between oxygenic photoautotrophs and heterotrophs related to the oxidative stress response as transcriptional patterns suggested that Synechococcus 7002 rather than Shewanella W3-18-1 provided scavenging functions for reactive oxygen species under co-culture conditions. This study provides an initial insight into the complexity of photoautotrophic-heterotrophic interactions and brings new perspectives of their role in the robustness and stability of the association.

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Growth of the Cyanobacterium Synechococcus leopoliensis CCAP1405/1 on Agar Media in the Presence of Heterotrophic Bacteria

Cited by 16 publications

References 38 publications

Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform

Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform

Phototrophic biofilm assembly in microbial-mat-derived unicyanobacterial consortia: model systems for the study of autotroph-heterotroph interactions

Inference of interactions in cyanobacterial–heterotrophic co-cultures via transcriptome sequencing

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