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Sulphide Resistance in the Cyanobacterium Microcystis aeruginosa: a Comparative Study of Morphology and Photosynthetic Performance Between the Sulphide-Resistant Mutant and the Wild-Type Strain

  • Environmental Microbiology
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Abstract

The cyanobacterium Microcystis aeruginosa is a mesophilic freshwater organism, which cannot tolerate sulphide. However, it was possible to isolate a sulphide-resistant (S r) mutant strain that was able to survive in a normally lethal medium sulphide. In order to evaluate the cost of the mutation conferring sulphide resistance in the S r strain of M. aeruginosa, the morphology and the photosynthetic performance were compared to that found in the wild-type, sulphide-sensitive (S s) strain. An increase in size and a disrupted morphology was observed in S r cells in comparison to the S s counterpart. Phycoerythrin and phycocyanin levels were higher in the S r than in the S s cells, whereas a higher carotenoid content, per unit volume, was found in the S s strain. The irradiance-saturated photosynthetic oxygen-production rate (GPR max) and the photosynthetic efficiency (measured both by oxygen production and fluorescence, α GPR and α ETR) were lower in the S r strain than in the wild-type. These results appear to be the result of package effect. On the other hand, the S r strain showed higher quantum yield of non-photochemical quenching, especially those regulated mechanisms (estimated throughout q N and Y(NPQ)) and a significantly lower slope in the maximum quantum yield of light-adapted samples (F v ′/F m ′) compared to the S s strain. These findings point to a change in the regulation of the quenching of the transition states (q T ) in the S r strain which may be generated by a change in the distribution of thylakoidal membranes, which somehow could protect metalloenzymes of the electron transport chain from the lethal effect of sulphide.

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Abbreviations

a*:

Chlorophyll-specific optical absorption cross section

Chla :

Chlorophyll a

E :

Incident irradiance

E 0.5 :

Half-saturation irradiance

ETR :

Electron transport rate computed as Y(II) × E × a* × 0.5

F 0 :

Minimal fluorescence of dark-adapted cells

F 0′:

Minimal fluorescence of illuminated cells

F t :

Steady-state fluorescence

F m :

Maximal fluorescence of dark-adapted cells

F m ′:

Maximal fluorescence of illuminated cells

F v :

Variable fluorescence of dark-adapted cells computed as F m  − F 0

F v ′:

Variable fluorescence of illuminated cells computed as F m ′ − F 0′

F v /F m :

Maximum quantum yield of dark-adapted cells computed as (F m   − F 0) / F m

F v ′/F m ′:

Maximum quantum yield of illuminated cells computed as (F m ′ − F 0′) / F m ′

GPR :

Gross photosynthetic oxygen-production rate

GPR max :

Irradiance-saturated GPR

NPQ :

Non-photochemical quenching parameter computed as Y(NPQ) / Y(NO)

PC:

Phycocyanin

PE:

Phycoerythrin

q E :

Energy-dependent quenching coefficient

q I :

Photoinhibitory quenching coefficient

q N :

Non-photochemical quenching coefficient computed as 1 − [(F m ′ − F 0′) / (F m  − F 0)]

q P :

Photochemical quenching coefficient computed as (F m ′ − F t ) / (F m ′ − F 0′)

q T :

Quenching associated with “state 1–state 2” transition

S r :

Sulphide-resistant (strain)

S s :

Sulphide-sensitive (strain)

TC:

Total carotenoids

Y(II):

Photochemical efficiency of PSII computed as (F m′ - F t)/F m′

Y(NO):

Quantum yield of non-regulated non-photochemical quenching computed as F t  / F m

Y(NPQ):

Quantum yield of regulated non-photochemical quenching computed as (F t  / F m ′) − (F t  / F m )

α ETR :

Photosynthetic efficiency calculated from ETR-E relationship

α GPR :

Photosynthetic efficiency calculated from GPR-E relationship

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Acknowledgments

This work was financially supported by the projects UMA-FEDER 2014–15 (FC14-CGL-08) and Ministerio de Economía y Competitividad (CGL2014-53862-P). The acquisition of the FlowCAM by the University of Málaga was co-financed by the 2008–2011 FEDER programme for Scientific-Technique Infrastructure (UNMA08-1E005). We thank Dr. Douglas Campbell and an anonymous reviewer for their suggestions to improve the manuscript. Dr. Eric C. Henry kindly revised the English style and usage.

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Authors and Affiliations

  1. Departamento de Biología Vegetal, Facultad de Ciencias, Universidad de Málaga, Campus de Teatinos s/n, E-29071, Málaga, Spain

    Elena Bañares-España, María del Mar Fernández-Arjona, María Jesús García-Sánchez & Antonio Flores-Moya

  2. Departamento de Química Analítica, Facultad de Ciencias, Universidad de Málaga, Campus de Teatinos s/n, E-29071, Málaga, Spain

    Miguel Hernández-López

  3. Departamento de Ecología y Geología, Facultad de Ciencias, Universidad de Málaga, Campus de Teatinos s/n, E-29071, Málaga, Spain

    Andreas Reul

  4. Departamento de Productos Naturales, Biología Vegetal y Edafología, Facultad de Farmacia, Universidad de Barcelona, Av. Joan XXIII s/n, 08028, Barcelona, Spain

    Mariona Hernández Mariné

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  1. Elena Bañares-España
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Correspondence to Elena Bañares-España.

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Bañares-España, E., del Mar Fernández-Arjona, M., García-Sánchez, M.J. et al. Sulphide Resistance in the Cyanobacterium Microcystis aeruginosa: a Comparative Study of Morphology and Photosynthetic Performance Between the Sulphide-Resistant Mutant and the Wild-Type Strain. Microb Ecol 71, 860–872 (2016). https://doi.org/10.1007/s00248-015-0715-3

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