Experimental evidence for the role of heterotrophic bacteria in the formation of Microcystis colonies

Abstract

Microcystis, a genus of cyanobacteria that is dominant in eutrophic lakes, occurs mainly as colonial morphs under natural conditions but as single cells in laboratory cultures. Recent studies have suggested that Microcystis-bacteria interactions significantly influence Microcystis morphology, but the underlying mechanism remains unclear. In this study, a total of 48 strains of heterotrophic bacteria were purified from Microcystis mucilage. Five bacteria, Aeromonas veronii, Enterobacter aerogenes, Exiguobacterium acetylicum, Bacillus cereus and Shewanella putrefaciens, can induce unicellular Microcystis to form colonies. Heterotrophic bacteria stimulated Microcystis growth and induced the production of extracellular polymeric substances in coculture treatments. Extracellular polymeric substances, such as extracellular polysaccharides (EPS), were responsible for the mucilage formation in colonial Microcystis. We analysed extracellular metabolic compounds produced by Microcystis aeruginosa and Microcystis wesenbergii using gas chromatography mass spectrometry. Filtrate extracts from coculture treatments indicated that some compounds, such as 2-dodecen-1-yl(-) s u c c i n i c a n h y d r i d e a n d b e n z o i c a c i d , 2 , 3 -bis[(trimethylsilyl)oxy]-, trimethylsilyl ester, might play a significant role in colonial M. aeruginosa or M. wesenbergii formation. Our data suggested that the interaction of Microcystis and heterotrophic bacteria was crucial for the formation of Microcystis colony and outbreak of Microcystis blooms.

Effects of the cultivable bacteria attached toMicrocystiscolonies on the colony size and growth ofMicrocystis

“…Sphingopyxis, Sphingomonas, Stenotrophomonas, Pseudomonas, Rheinheimera and Chryseobacterium (the closest genus of the bacterial isolates QW20, QW04, QW19, QW15, QW02 and QW12, respectively) have been previously detected in Microcystis colonies harvested from Lake Taihu (Cai et al 2014;Shi et al 2010). Aeromonas, Exiguobacterium and Bacillus (the closest genus of the bacterial isolates QW14, QW05 and QW08, respectively) are present in Microcystis colonies collected from Lake Taihu, Lake Dianchi and Lake Donghu (China) (Wang et al 2016). Delftia (the closest genus of the bacterial isolate QW 07) is associated with Microcystis blooms occurred in water bodies of Germany, India, Portugal, Wisconsin (USA) and China (Dziallas and Grossart 2011).…”

“…Sphingomonas is associated with Microcystis in all the samples from laboratory batch experiments, close-to field experiments and water bodies of Germany, India, Portugal, Wisconsin (USA) and China, and thus is considered to be an integral element of Microcystis blooms (Dziallas and Grossart 2011). Extracellular polysaccharide (EPS) is considered to be involved in the formation of Microcystis colony (Wang et al 2016). Two compounds tetradecamethylhexasiloxane and octamethylcyclotetrasiloxane which play a crucial role in polymer formation have been previously found in a Microcystis-associated bacterium Shewanella putrefaciens (Wang et al 2016).…”

“…Extracellular polysaccharide (EPS) is considered to be involved in the formation of Microcystis colony (Wang et al 2016). Two compounds tetradecamethylhexasiloxane and octamethylcyclotetrasiloxane which play a crucial role in polymer formation have been previously found in a Microcystis-associated bacterium Shewanella putrefaciens (Wang et al 2016). It might be speculated that certain Microcystis-attached bacteria may stimulate the excretion of Microcystis EPS through producing bioactive compounds, and in turn increase the colony size of Microcystis.…”

“…Microcystindegrading bacteria have been found in the mucilage of Microcystis colonies (Maruyama et al 2003). Bacteria attached to Microcystis colonies may induce unicellular Microcystis to form colonies (Shen et al 2011;Wang et al 2016). have reported that bacterial strains isolated from the mucilage of Microcystis colonies influence the growth of unicellular M. aeruginosa positively or negatively.…”

Increased algicidal activity of Aeromonas veronii in response to Microcystis aeruginosa: interspecies crosstalk and secondary metabolites synergism

“…Numerous studies have uncovered interspecies interactions between cyanobacteria and bacteria (Ostensvik et al, 1998;Gross, 2003;Hulot and Huisman, 2004;Babica et al, 2006;Leao et al, 2009;Yuan et al, 2009;Parveen et al, 2013;Yang et al, 2013;Penn et al, 2014;Bittencourt-Oliveira et al, 2015;Allen et al, 2016;Briand et al, 2016;Van Wichelen et al, 2016;Wang et al, 2016;Dias et al, 2017;Otten et al, 2017;Wu et al, 2017;Ndlela et al, 2018;Sun et al, 2018;Woodhouse et al, 2018;Xu et al, 2018;Yu et al, 2019 and references therein), but the nature of the allelochemicals and the mechanisms involved in the interactions are in most cases poorly understood. We aimed at gaining a better understanding of the interspecies interaction between Microcystis sp.…”