Temporal and functional interrelationships between bacterioplankton communities and the development of a toxigenic Microcystis bloom in a lowland European reservoir

Abstract

The cyanobacteria-associated microbiome is constantly reshaped by bloom development. However, the synergistic-antagonistic nature of the relationships between Microcystis and its microbiome still remains unclear. Therefore, temporal changes of bacterioplankton communities and their functional potential through different developing stages of a Microcystis toxigenic bloom were investigated, considering bacterioplankton assemblages as particle-attached (PAB) and free-living (FLB) bacteria. 16S rRNA sequencing revealed that PAB were represented by Proteobacteria and Cyanobacteria, while FLB by Proteobacteria and Actinobacteria. Network and ordination analyses indicated that PAB inter-relationships were more complex—numerous connections between taxa with stronger correlations, than FLB—rather influenced by physico-chemical parameters. PAB in pre-summer was diverse with Proteobacteria containing potential taxa involved in nitrogen-transforming processes. In mid-summer, PAB presented a mix-bloom dominated by Snowella, Aphanizomenon, and Microcystis, which were succeeded by toxigenic Microcystis in post-summer. Both periods were associated to potential taxa with parasitic/predatory lifestyles against cyanobacteria. In post-summer, Sutterellaceae were recognized as poor water quality indicators, and their strong association with Microcystis could have represented an increased threat for that period. Microcystis was a major factor significantly reducing PAB diversity and evenness, suggesting that it negatively influenced bacterioplankton assemblages, probably also altering the overall community functional potential.

Cyanobacterial Harmful Bloom Lipopolysaccharides Induce Pro-Inflammatory Effects in Immune and Intestinal Epithelial Cells In Vitro

“…However, these earlier measurements were performed by an LAL assay [ 41 ] that found for LPSs from Microcystis on average 13-times-higher endotoxin activities than those of the PyroGene™ assay [ 1 ], and this phenomenon could possibly occur also to LPSs isolated from other cyanobacterial species. However, the differences among endotoxin activities between different samples and studies could be most likely attributed to different taxonomical compositions of respective water blooms, including cyanobacteria as well as associated G- bacteria, which show qualitative and quantitative variations depending on the season, environmental factors, cyanobacterial species, or oligotype [ 8 , 9 , 10 , 42 ]. Different cyanobacterial as well as G- bacterial species, strains, genotypes, or serotypes can exhibit major differences in their LPS structures [ 6 , 12 , 13 ], and also their endotoxin activities can differ by several orders of magnitude [ 1 , 41 , 43 ].…”

“…On the other hand, there are also bacterial species with LPSs bearing anti-inflammatory activity, e.g., Rhodobacter sphaeroides [ 49 ] whose LPS is commercially available as an antagonist for TLR4 (InVivogen). As the microbial community of water blooms is very diverse and dynamic [ 8 , 9 , 10 , 42 , 50 ], various G- bacteria can be present in the studied biomasses and the pro- and anti-inflammatory properties of the LPSs can manifest and support or weaken each other in the environmental mixture. Moreover, different cyanobacterial LPSs can also elicit either pro- or anti-inflammatory effects [ 2 ].…”

“…Therefore, LPSs are inherently present in any locality with CyanoHAB occurrence [ 6 , 7 ]. In addition to cyanobacterial LPSs, heterotrophic G- bacteria are naturally associated with CyanoHABs and interact with cyanobacteria [ 8 , 9 , 10 ], representing another source of LPSs during CyanoHAB events. In some instances, pathogenic G- bacterial species, e.g., Acinetobacter , Pseudomonas , Aeromonas , or Vibrio , were detected in CyanoHABs [ 11 ].…”

Stringent Response of Cyanobacteria and Other Bacterioplankton during Different Stages of a Harmful Cyanobacterial Bloom

“…This finding marks a notable advancement in the field, aligning with the current trend of studies aimed at understanding the survival strategies of toxin-producing cyanobacteria under nutrient limitation. ,, Additionally, our observations reveal a profound shift in the phytoplanktonic community, accompanied by the identification of various genes and metabolic pathways that contribute to this adaptive response (Figures S2 and and ). These complex processes and the progression of the microbial community play a critical role in the effective utilization of N and P in the lake, thereby significantly impacting the ecosystem’s structure and functioning. , Unfortunately, the proliferation of multiple genotypes capable of toxin production exacerbates cyanoHABs formation. − While we have identified cyanobacteria’s resilience to environmental changes as a primary driver of their dominance in the microbial community during the bloom, the exact mechanisms governing the stringent response and interactions between cyanobacteria and coexisting bacterioplankton remain elusive, apart from alterations in abundance and gene expression profiles. − Further investigation is needed to understand the synergistic–antagonistic nature of their relationships and explore potential mechanisms for suppressing or terminating the bloom.…”

Vertical distribution and seasonal dynamics of planktonic cyanobacteria communities in a water column of deep mesotrophic Lake Geneva

“…Less is known about the effects of cyanobacteria on bacterioplankton communities and their functions in mesotrophic and oligotrophic environments. However, studies available to date, developed mostly in eutrophic lakes and reservoirs, have noted an impact of cyanobacteria such as Microcystis aeruginosa on bacterioplankton composition and succession ( Zheng et al, 2008 ; Guedes et al, 2018 ; Mankiewicz-Boczek and Font-Nájera, 2022 ).…”