Abstract
Secondary metabolites of bacteria are regulatory molecules that act as “info-chemicals” that control some metabolic processes in the cells of microorganisms. These molecules provide the function of bacteria communication in microbial communities. As primary producers of organic matter in the biosphere, microalgae play a central ecological role in various ecosystems. Photosynthesis is a central process in microalgae cells, and it is exposed to various biotic and abiotic factors. Various secondary metabolites of bacteria confer a noticeable regulatory effect on photosynthesis in microalgae cells. The main purpose of this review is to highlight recent experimental results that demonstrate the impact of several types of common bacterial metabolites (volatile organic compounds, non-protein amino acids, and peptides) on photosynthetic activity in cells of microalgae. The use of these molecules as herbicides can be of great importance both for practical applications and for basic research.
Similar content being viewed by others
References
Alfiky A, Weisskopf L (2021) Deciphering Trichoderma–plant–pathogen interactions for better development of biocontrol applications. J Fungi 7(1):61. https://doi.org/10.3390/jof7010061
Artiga M (2021) Bacterial communication. Biol Philos 36(4). https://doi.org/10.1007/s10539-021-09814-1
Babica P, Bláha L, Maršálek B (2006) Exploring the natural role of microcystins – a review of effects on photoautotrophic organisms. J Phycol 42:9–20. https://doi.org/10.1111/j.1529-8817.2006.00176.x
Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622. https://doi.org/10.1093/jxb/erg076
Balfagón D, Gómez-Cadenas A, Rambla JL, Granell A, de Ollas C, Bassham DC, Mittler R, Zandalinas SI (2022) γ-Aminobutyric acid plays a key role in plant acclimation to a combination of high light and heat stress. Plant Physiol. https://doi.org/10.1093/plphys/kiac010
Banin E, Khare SK, Naider F, Rosenberg E (2001) Proline-rich peptide from the coral pathogen Vibrio shiloi that inhibits photosynthesis of zooxanthellae. Appl Environ Microbiol 67:1536–1541. https://doi.org/10.1128/AEM.67.4.1536-1541.2001
Berntzon L, Erasmie S, Celepli N, Eriksson J, Rasmussen U, Bergman B (2013) BMAA inhibits nitrogen fixation in the cyanobacterium Nostoc sp. PCC 7120. Mar Drugs 11:3091–3108. https://doi.org/10.3390/md11083091
Blum U (2011) Plant–plant allelopathic interactions. Plant-Plant Allelopathic Interact 1–7. https://doi.org/10.1007/978-94-007-0683-5_1
Brenner ED, Martinez-Barboza N, Clark AP, Liang QS, Stevenson DW, Coruzzi GM (2000) Arabidopsis mutants resistant to S(+)-beta-methyl-alpha, beta-diaminopropionic acid, a cycad-derived glutamate receptor agonist. Plant Physiol 124:1615–1624. https://doi.org/10.1104/pp.124.4.1615
Brenner ED, Feinberg P, Runko S et al (2009) A mutation in the Proteosomal Regulatory Particle AAA-ATPase-3 in Arabidopsis impairs the light-specific hypocotyl elongation response elicited by a glutamate receptor agonist, BMAA. Plant Mol Biol 70:523–533. https://doi.org/10.1007/s11103-009-9489-7
Campos A, Redouane EM, Freitas M, Amaral S, Azevedo T, Loss L, Máthé C, Mohamed ZA, Oudra B, Vasconcelos V (2021) Impacts of microcystins on morphological and physiological parameters of agricultural plants: a review. Plants (Basel) 10:639. https://doi.org/10.3390/plants10040639
Casagrande DJ, Given PH (1980) Geochemistry of amino acids in some Florida peat accumulation-II. Amino acid distributions. Geochim Cosmochim Acta 44:1493–1507. https://doi.org/10.1016/0016-7037(80)90114-3
Chang DW, Hsieh ML, Chen YM, Lin TF, Chang JS (2011) Kinetics of cell lysis for Microcystis aeruginosa and Nitzschia palea in the exposure to β-cyclocitral. J Hazard Mater 185:1214–1220. https://doi.org/10.1016/j.jhazmat.2010.10.033
Chen Y, Weng Y, Zhou M, Meng Y, Liu J, Yang L, Zuo Z (2019) Linalool- and α-terpineol-induced programmed cell death in Chlamydomonas reinhardtii. Ecotoxicol Environ Saf 167:435–440. https://doi.org/10.1016/j.ecoenv.2018.10.062
Cheng F, Cheng Z (2015) Research progress on the use of plant allelopathy in agriculture and the physiological and ecological mechanisms of allelopathy. Front Plant Sci 6. https://doi.org/10.3389/fpls.2015.01020
Chlipala GE, Mo S, Orjala J (2011) Chemodiversity in freshwater and terrestrial cyanobacteria - a source for drug discovery. Curr Drug Targets 12:1654–1673. https://doi.org/10.2174/138945011798109455
Czárán T, Hoekstra RF (2009) Microbial communication, cooperation and cheating: quorum sensing drives the evolution of cooperation in bacteria. PLoS ONE 4(8):e6655. https://doi.org/10.1371/journal.pone.0006655
Dawson RM (1998) The toxicology of microcystins. Toxicon 36:953–962. https://doi.org/10.1016/S0041-0101(97)00102-5
Downing TG, Phelan RR, Downing S (2015) A potential physiological role for cyanotoxins in cyanobacteria of arid environments. J Arid Environ 112:147–151. https://doi.org/10.1016/j.jaridenv.2014.02.005
Downing S, Downing TG (2016) The metabolism of the non proteinogenic amino acid β-N-methylamino-L-alanine (BMAA) in the cyanobacterium Synechocystis PCC 6803. Toxicon 115:41–48. https://doi.org/10.1016/j.toxicon.2016.03.005
Fichtner M, Voigt K (1861) Schuster S (2017) The tip and hidden part of the iceberg: proteinogenic and non-proteinogenic aliphatic amino acids. Biochim Biophys Acta Gen Subj 1 Pt A:3258–3269. https://doi.org/10.1016/j.bbagen.2016.08.008
Forchhammer K, Lüddecke J (2015) Sensory properties of the P II signalling protein family. FEBS J 283:425–437. https://doi.org/10.1111/febs.13584
Forchhammer K, Selim KA (2019) Carbon/nitrogen homeostasis control in cyanobacteria. FEMS Microbiol Rev 44:33–53. https://doi.org/10.1093/femsre/fuz025
Gantar M, Berry JP, Thomas S et al (2008) Allelopathic activity among cyanobacteria and microalgae isolated from Florida freshwater habitats. FEMS Microbiol Ecol 64:55–64. https://doi.org/10.1111/j.1574-6941.2008.00439.x
García-Cerdán JG, Kovács L, Tóth T et al (2010) The PsbW protein stabilizes the supramolecular organization of II in higher plants. Plant J 65:368–381. https://doi.org/10.1111/j.1365-313x.2010.04429.x
Hartmann T (2008) The lost origin of chemical ecology in the late 19th century. Proc Natl Acad Sci U S A 105:4541–4546. https://doi.org/10.1073/pnas.0709231105
Havaux M (2020) β-Cyclocitral and derivatives: emerging molecular signals serving multiple biological functions. Plant Physiol Biochem 155:35–41. https://doi.org/10.1016/j.plaphy.2020.07.032
Heisey RM (1990) Allelopathic and herbicidal effects of extracts from tree of heaven (Ailanthus altissima). Am J Bot 77:662–670. https://doi.org/10.2307/2444812
Hesse K, Dittmann E, Bӧrner T (2001) Consequences of impaired microcystin production for light-dependent growth and pigmentation of Microcystis aeruginosa PCC 7806. FEMS Microbiol Ecol 37:39–43. https://doi.org/10.1016/s0168-6496(01)00142-8
Huang H, Xiao X, Ghadouani A, Wu J, Nie Z, Peng C, Xu X, Shi J (2015) Effects of natural flavonoids on photosynthetic activity and cell integrity in Microcystis aeruginosa. Toxins (Basel) 7:66–80. https://doi.org/10.3390/toxins7010066
Jander G, Kolukisaoglu U, Stahl M, Yoon GM (2020) Editorial: Physiological aspects of non-proteinogenic amino acids in plants. Front Plant Sci 11:519464. https://doi.org/10.3389/fpls.2020.519464
Janssen EM-L (2019) Cyanobacterial peptides beyond microcystins – a review on co-occurrence, toxicity, and challenges for risk assessment. Water Res 151:488–499. https://doi.org/10.1016/j.watres.2018.12.048
Jiang Z, Peiyong G, Chang C, Gao L, Li S, Wan J (2014) Effects of allelochemicals from Ficus microcarpa on Chlorella pyrenoidosa. Braz Arch Biol Technol 57:595–605. https://doi.org/10.1590/S1982-88372014000100018
Jones MR, Pinto E, Torres MA, Dörr F, Mazur-Marzec H, Szubert K, … Janssen EM-L (2021) CyanoMetDB, a comprehensive public database of secondary metabolites from cyanobacteria. Water Res 196:117017. https://doi.org/10.1016/j.watres.2021.11701
Kaebernick M, Neilan BA (2001) Ecological and molecular investigations of cyanotoxin production. FEMS Microbiol Ecol 35:1–9. https://doi.org/10.1111/j.1574-6941.2001.tb00782.x
Koksharova OA (2020) Cyanobacterial VOCs as allelopathic tools. In: Weisskopf L, Piechulla B, Ryu CM (eds) Bacterial volatile compounds as mediators of airborne interactions. Springer, Singapore, pp 257–280. https://doi.org/10.1007/978-981-15-7293-7_11
Koksharova OA, Butenko IO, Pobeguts OV, Safronova NA, Govorun VM (2020) The first proteomic study of Nostoc sp. PCC 7120 exposed to cyanotoxin BMAA under nitrogen starvation. Toxins 12:310. https://doi.org/10.3390/toxins12050310
Koksharova OA, Butenko IO, Pobeguts OV, Safronova NA, Govorun VM (2020) Proteomic insights into starvation of nitrogen-replete cells of Nostoc sp. PCC7120 under BMAA treatment. Toxins 12:372. https://doi.org/10.3390/toxins12060372
Koksharova OA, Butenko IO, Pobeguts OV, Safronova NA, Govorun VM (2021) β-N-Methylamino-L-Alanine (BMAA) Causes severe stress in Nostoc sp. PCC 7120 cells under diazotrophic conditions: a proteomic study. Toxins 13:325. https://doi.org/10.3390/toxins13050325
Keating KI (1978) Blue-green algal inhibition of diatom growth: transition from mesotrophic to eutrophic community structure. Science 199:971–973. https://doi.org/10.1126/science.199.4332.971
Latif S, Chiapusio G, Weston LA (2017) Allelopathy and the role of allelochemicals in plant defence. Adv Bot Res 82:19–54. https://doi.org/10.1016/bs.abr.2016.12.001
Legrand C, Rengefors K, Fistarol GO et al (2003) Allelopathy in phytoplankton – biochemical, ecological and evolutionary aspects. Phycologia 42:406–419. https://doi.org/10.2216/i0031-8884-42-4-406.1
Lee J, Rai PK, Jeon YJ, Kim K-H, Kwon EE (2017) The role of algae and cyanobacteria in the production and release of odorants in water. Environ Pollut 227:252–262. https://doi.org/10.1016/j.envpol.2017.04.058
Lemfack MC, Gohlke BO, Toguem SMT, Preissner S, Piechulla B, Preissner R (2018) mVOC 2.0: a database of microbial volatiles. Nucleic Acids Res 46(D1):D1261–D1265. https://doi.org/10.1093/nar/gkx1016
Leão PN, Vasconcelos MT, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35:271–282. https://doi.org/10.3109/10408410902823705
Leu E, Krieger-Liszkay A, Goussias C, Gross EM (2002) Polyphenolic allelochemicals from the aquatic angiosperm Myriophyllum spicatum inhibit photosystem II. Plant Physiol 130(4):2011–2018. https://doi.org/10.1104/pp.011593
Li L, Dou N, Zhang H, Wu C (2021) The versatile GABA in plants. Plant Signal Behav 16(3):1862565. https://doi.org/10.1080/15592324.2020.1862565
Liu B, Zhou P, Tian J, Jiang S (2007) Effect of pyrogallol on the growth and pigment content of cyanobacteria-blooming toxic and nontoxic Microcystis aeruginosa. Bull Environ Contam Toxicol 78:499–502. https://doi.org/10.1007/s00128-007-9096-8
Liu J, Yu Q, Ye B, Zhu K, Yin J, Zheng T, Xu S, Sun Q, Li Y, Zuo Z (2021) Programmed cell death of Chlamydomonas reinhardtii induced by three cyanobacterial volatiles β-ionone, limonene and longifolene. Sci Total Environ 762:144539. https://doi.org/10.1016/j.scitotenv.2020.144539
Lobner D, Piana PMT, Salous AK, Peoples RW (2007) β-N-Methylamino-l-alanine enhances neurotoxicity through multiple mechanisms. Neurobiol Dis 25:360–366. https://doi.org/10.1016/j.nbd.2006.10.002
Makkar HPS, Siddhuraju P, Becker K (2007) Plant secondary metabolites. Methods in Molecular Biology™. doi:https://doi.org/10.1007/978-1-59745-425-4
Mantzouki E et al (2018) A European Multi Lake Survey dataset of environmental variables, phytoplankton pigments and cyanotoxins. Sci Data 5:180226. https://doi.org/10.1038/sdata.2018.226
Máthé C, M-Hamvas M, Vasas G, Garda T, Freytag C (2021) Subcellular alterations induced by cyanotoxins in vascular plants-a review. Plants (Basel) 10:984. https://doi.org/10.3390/plants10050984
Merel S et al (2013) State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int 59:303–327. https://doi.org/10.1016/j.envint.2013.06.013
Molisch H (1937) Der Einfluss einer Pflanze auf die andere: Allelopathie. Fischer, Jena
Ngwa FF, Madramootoo CA, Jabaji S (2014) Comparison of cyanobacterial microcystin synthetase (mcy) E gene transcript levels, mcy E gene copies, and biomass as indicators of microcystin risk under laboratory and field conditions. Microbiol Open 3:411–425. https://doi.org/10.1002/mbo3.173
Nunn PB (2017) 50 years of research on α-amino-β-methylaminopropionic acid (β-methylaminoalanine). Phytochemistry 144:271–281. https://doi.org/10.1016/j.phytochem.2017.10.002
Nunn PB, Codd GA (2019) Environmental distribution of the neurotoxin l-BMAA in Paenibacillus species. Toxicol Res. https://doi.org/10.1039/c9tx00203k
Omidi A, Esterhuizen-Londt M, Pflugmacher S (2017) Still challenging: the ecological function of the cyanobacterial toxin microcystin – what we know so far. Toxin Rev 37:87–105. https://doi.org/10.1080/15569543.2017.1326059
Pang Z, Chen J, Wang T et al (2021) Linking plant secondary metabolites and plant microbiomes: a review. Front Plant Sci 12:621276. https://doi.org/10.3389/fpls.2021.62127
Plyuta VA, Chernikova AS, Sidorova DE, Kupriyanova EV, Koksharova OA, Chernin LS, Khmel IA (2021) Modulation of Arabidopsis thaliana growth by volatile substances emitted by Pseudomonas and Serratia strains. World J Microbiol Biotechnol 37:82. https://doi.org/10.1007/s11274-021-03047-w
Popova AA, Koksharova OA, Lipasova VA, Zaitseva JV, Katkova-Zhukotskaya OA, Eremina SI, … Khmel IA (2014) Inhibitory and toxic effects of volatiles emitted by strains of Pseudomonas and Serratia on growth and survival of selected microorganisms, Caenorhabditis elegans, and Drosophila melanogaster. Biomed Res Int 2014:1–11. https://doi.org/10.1155/2014/125704
Popova AA, Koksharova OA (2016) Neurotoxic non-proteinogenic amino acid β-N-methylamino-L-alanine and its role in biological systems. Biochemistry 81:794–805. https://doi.org/10.1134/S0006297916080022
Popova A, Rasmussen U, Semashko T, Govorun V, Koksharova O (2018) Stress effects of cyanotoxin β-methylamino-L-alanine (BMAA) on cyanobacterial heterocyst formation and functionality. Environ Microbiol Rep 10:369–377. https://doi.org/10.1111/1758-2229.12647
Popova A, Semashko T, Kostina N, Rasmussen U, Govorun V, Koksharova O (2018b) The cyanotoxin BMAA induces heterocyst specific gene expression in Anabaena sp. PCC 7120 under repressive conditions. Toxins 10. doi:https://doi.org/10.3390/toxins10110478.
Ren S (2008) Allelopathy in sustainable agriculture and forestry. Springer Science (Business Media), New York. https://doi.org/10.1007/978-0-387-77337-7
Reyes-Sosa FM, Gil-Martínez J, Molina-Heredia FP (2011) Cytochrome c 6-like protein as a putative donor of electrons to photosystem I in the cyanobacterium Nostoc sp. PCC 7119. Photosynth Res 110:61–72. https://doi.org/10.1007/s11120-011-9694-5
Rice EL (1984) Allelopathy, 2nd edn. Academic Press, New York, p 422. https://doi.org/10.1016/S0031-9422(00)80730-X
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61. https://doi.org/10.1099/00221287-111-1-1
Ryu C-M, Weisskopf L, Piechulla B (Eds) (2020) Bacterial volatile compounds as mediators of airborne interactions. Springer Nature Singapore Singapore, 320, https://doi.org/10.1007/978-981-15-7293-7
Schandry N, Becker C (2020) Allelopathic plants: models for studying plant–interkingdom interactions. Trends Plant Sci 25:176–185. https://doi.org/10.1016/j.tplants.2019.11.004
Sedmak B, Eleršek T (2006) Microcystins induce morphological and physiological changes in selected representative phytoplanktons. Microb Ecol 51:508–515. https://doi.org/10.1007/s00248-006-9045-9
Shao J, Wu X, Li R (2009) Physiological responses of Microcystis aeruginosa PCC7806 to nonanoic acid stress. Environ Toxicol 24:610–617. https://doi.org/10.1002/tox.20462
Shenker M, Fan TWM, Crowley DE (2001) Phytosiderophores influence on cadmium mobilization and uptake by wheat and barley plants. J Environ Qual 30:2091–2098. https://doi.org/10.2134/jeq2001.2091
Shi L, Carmichael WW, Miller I (1995) Immuno-gold localization of hepatotoxins in cyanobacterial cells. Arch Microbiol 163:7–15. https://doi.org/10.1007/BF00262197
Sidorova DE, Plyuta VA, Padiy DA, Kupriyanova EV, Roshina NV, Koksharova OA, Khmel IA (2022) The effect of volatile organic compounds on different organisms: agrobacteria, plants and insects. Microorganisms 10:69. https://doi.org/10.3390/microorganisms10010069
Singh DP, Tyagi MB, Arvind Kumar JK et al (2001) Antialgal activity of a hepatotoxin-producing cyanobacterium Microcystis aeruginosa. World J Microbiol Biotechnol 17:15–22. https://doi.org/10.1023/A:1016622414140
Singh JS (2016) Cyanobacteria: a precious bio-resource in agriculture, ecosystem, and environmental sustainability. Front Microbiol 7:529. https://doi.org/10.3389/fmicb.2016.00529
Sun Q, Zhou M, Zuo Z (2020) Toxic mechanism of eucalyptol and β-cyclocitral on Chlamydomonas reinhardtii by inducing programmed cell death. J Hazard Mater 389:121910. https://doi.org/10.1016/j.jhazmat.2019.121910
Svirčev Z, Lalić D, Bojadžija Savić G, Tokodi N et al (2019) Global geographical and historical overview of cyanotoxin distribution and cyanobacterial poisonings. Arch Toxicol. https://doi.org/10.1007/s00204-019-02524-4
Tabita FR, Colletti C (1979) Carbon dioxide assimilation in cyanobacteria: regulation of ribulose, 1,5-bisphosphate carboxylase. J Bacteriol 140:452–458. https://doi.org/10.1128/jb.140.2.452-458.1979
Torrado A, Ramírez-Moncayo C, Navarro JA, Mariscal V, Molina-Heredia FP (2019) Cytochrome c6 is the main respiratory and photosynthetic soluble electron donor in heterocysts of the cyanobacterium Anabaena sp. PCC 7120. Biochim Biophys Acta BBA Bioenergy 1860:60–68. https://doi.org/10.1016/j.bbabio.2018.11.009
Voronova EN, Konyukhov IV, Koksharova OA, Popova AA, Pogosyan SI, Khmel IA, Rubin AB (2019) Inhibition of cyanobacterial photosynthetic activity by natural ketones. J Phycol. https://doi.org/10.1111/jpy.12861
Vranova V, Rejsek K, Skene KR, Formanek P (2011) Non-protein amino acids: plant, soil and ecosystem interactions. Plant Soil 342:31–48. https://doi.org/10.1007/s11104-010-0673-y
Walsh CT, O’Brien RV, Khosla C (2013) Nonproteinogenic amino acid building blocks for nonribosomal peptide and hybrid polyketide scaffolds. Angew Chem Int Ed 52:7098–7124. https://doi.org/10.1002/anie.201208344
Wang H, Zhu H, Zhang L, Xue W, Yuan B (2014) Identification of antialgal compounds from the aquatic plant Elodea nuttallii. Allelopath J 34:207–213
Watson SB (2003) Cyanobacterial and eukaryotic algal odor compounds: signals or by-products? A review of their biological activity. Phycologia 42:332–350. https://doi.org/10.2216/i0031-8884-42-4-332.1
Wink M (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theoret Appl Genetics 75:225–233. https://doi.org/10.1007/BF00303957
Welker M, Von Döhren H (2006) Cyanobacterial peptides-nature’s own combinatorial biosynthesis. FEMS Microbiol Rev 30:530–563. https://doi.org/10.1111/j.1574-6976.2006.00022.x
Xie Y, Tian L, Han X, Yang Y (2021) Research advances in allelopathy of volatile organic compounds (VOCs) of plants. Horticulturae 7:278. https://doi.org/10.3390/horticulturae7090278
Xu Q, Yang L, Yang W, Bai Y, Hou P, Zhao J et al (2017) Volatile organic compounds released from Microcystis flos-aquae under nitrogen sources and their toxic effects on Chlorella vulgaris. Ecotoxicol Environ Saf 135:191–200. https://doi.org/10.1016/j.ecoenv.2016.09.027
Yamashita R, Bober B, Kanei K, Arii S, Tsuji K, Harada KI (2020) Analytical technique optimization on the detection of β-cyclocitral in Microcystis species. Molecules 25:832. https://doi.org/10.3390/molecules25040832
Yazaki K, Arimura G, Ohnishi T (2017) ‘Hidden’ terpenoids in plants: their biosynthesis, localization and ecological roles. Plant Cell Physiol 58:1615–1621. https://doi.org/10.1093/pcp/pcx123
Young FM, Thomson C, Metcalf JS et al (2005) Immunogold localization of microcystins in cryosectioned cells of Microcystis. J Struct Biol 151:208–214. https://doi.org/10.1016/j.jsb.2005.05.007
Young FM, Morrison LF, James J et al (2008) Quantification and localization of microcystins in colonies of a laboratory strain of Microcystis (Cyanobacteria) using immunological methods. Eur J Phycol 43:217–225. https://doi.org/10.1080/09670260701880460
Zer H, Mizrahi H, Malchenko N, Avin-Wittenberg T, Klipcan L, Ostersetzer-Biran O (2020) The phytotoxicity of meta-tyrosine is associated with altered phenylalanine metabolism and misincorporation of this non-proteinogenic Phe-analog to the plant’s proteome. Front Plant Sci 11:140. https://doi.org/10.3389/fpls.2020.00140
Zervou S-K, Moschandreou K, Paraskevopoulou A et al (2021) Cyanobacterial toxins and peptides in Lake Vegoritis. Greece Toxins 13(6):394. https://doi.org/10.3390/toxins13060394
Zhang T, Zheng C, He M, Wu A, Nie L (2009) Inhibition on algae of fatty acids and the structure-effect relationship. China Environ Sci 29:274–279
Zhang Y, Vo Duy S, Munoz G, Sauvé S (2022) Phytotoxic effects of microcystins, anatoxin-a and cylindrospermopsin to aquatic plants: a meta-analysis. Sci Total Environ 810:152104. https://doi.org/10.1016/j.scitotenv.2021.152104
Zhao J, Yang L, Zhou L, Bai Y, Wang B, Hou P, Xu Q, YangW ZZ (2016) Inhibitory effects of eucalyptol and limonene on the photosynthetic abilities in Chlorella vulgaris (Chlorophyceae). Phycologia 55:696–702. https://doi.org/10.2216/16-38.1
Zhu J, Liu B, Wang J, Gao Y, Wu Z (2010) Study on the mechanism of allelopathic influence on cyanobacteria and chlorophytes by submerged macrophyte (Myriophyllum spicatum) and its secretion. Aquat Toxicol 98:196–203. https://doi.org/10.1016/j.aquatox.2010.02.011
Zhu X, Dao G, Tao Y, Zhan X, Hu H (2021) A review on control of harmful algal blooms by plant-derived allelochemicals. J Hazard Mater 401:123403. https://doi.org/10.1016/j.jhazmat.2020.123403
Zuo Z, Yang Y, Xu Q, Yang W, Zhao J, Zhou L (2018) Effects of phosphorus sources on volatile organic compound emissions from Microcystis flos-aquae and their toxic effects on Chlamydomonas reinhardtii. Environ Geochem Health 40:1283. https://doi.org/10.1007/s10653-017-0055-y
Acknowledgements
The authors were inspired to write this review by the work of the VIII Congress of the Russian Photobiological Society, All-Russian Conference “Modern problems of Photobiology.” The authors are grateful to the unknown reviewers for valuable comments that contributed to the improvement of the text of the manuscript.
Funding
The study was supported by state program no. AAAA-A17-117120570011–4 (“Investigation of the mechanism of energy conversion by photosynthesis enzymes”).
Author information
Authors and Affiliations
Contributions
Koksharova Olga had the idea for the article, performed the literature search and data analysis, and drafted and critically revised the work. Safronov Nikolai critically revised the work and made an illustration. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
This article does not contain any studies with animals performed by any of the authors.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Koksharova, O.A., Safronov, N.A. The effects of secondary bacterial metabolites on photosynthesis in microalgae cells. Biophys Rev 14, 843–856 (2022). https://doi.org/10.1007/s12551-022-00981-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12551-022-00981-3