Phenology and ecological role of Aerobic Anoxygenic Phototrophs in fresh waters

Abstract

Aerobic anoxygenic phototrophic (AAP) bacteria are heterotrophic bacteria that supply their metabolism with light energy harvested by bacteriochlorophyll-a-containing reaction centres. Despite their substantial contribution to bacterial biomass, microbial food webs and carbon cycle, their phenology in freshwater lakes remains unknown. Hence, we investigated seasonal variations of AAP abundance and community composition biweekly across three years in a temperate, meso-oligotrophic freshwater lake. AAP bacteria displayed a clear seasonal trend with a spring maximum following the bloom of phytoplankton and a secondary maximum in autumn. As the AAP bacteria represent a highly diverse assemblage of species, we followed their seasonal succession using the amplicon sequencing of thepufM marker gene. To enhance the accuracy of the taxonomic assignment, we developed newpufM primers that generate longer amplicons and compiled the currently largest database ofpufM gene, comprising 3633 reference sequences spanning all phyla known to contain AAP species. With this novel resource we demonstrated recurrent and dynamic seasonal succession of the AAP community. The majority of the species appeared during specific phases of the seasonal cycle, with less than 2% of AAP species detected during the whole year. Our results document the indigenous freshwater nature of the AAP community, characterized by high resilience and heterogenic adaptations to varying conditions of the freshwater environment. By integrating this information with the indicator of primary production (Chlorophyll-a) and existing ecological models, we show that AAP bacteria play a pivotal role in the recycling of dissolved organic matter released during spring phytoplankton bloom, contributing significantly to the ecological dynamics of lakes.

Effects of excess phosphate on a coastal plankton community: a mesocosm experiment in the Baltic Sea

“…Under all conditions AAP bacteria demonstrated higher growth rates compared to the general heterotrophic bacteria, especially in the N-add treatment. The phytoplankton spring bloom have been shown to enhance AAP bacteria proliferation in fresh waters (Villena-Alemany et al, 2023), and our results support that AAP bacteria are impacted by the phosphorous and nitrogen availability (Mašín et al, 2012) and has potential in phosphate removal.…”

“…Heterotrophic bacteria were detected according to their green fluorescence and side scatter properties using FACSDiva Software (BD Biosciences). In addition, aerobic anoxygenic phototrophic (AAP) bacteria were counted using the bacteriochlorophyll- a fluorescence in epifluorescence microscope according to Villena-Alemany et al (2023).…”

Winners in good times and bad times: Aerobic anoxygenic phototrophic bacteria profit from photoheterotrophy under carbon-rich and poor conditions

“…Limnohabitans ) are considered copiotrophs (Chiriac et al ., 2023, Park et al ., 2023). Furthermore, in June AAP bacteria grew faster than the heterotrophic bacteria in all treatments, providing experimental support for the recently suggested inclusion of AAP bacteria in the Phytoplankton Ecology Group (PEG) model as super competitors profiting from spring phytoplankton bloom (Villena-Alemany et al ., 2023b). However, the negligible growth of AAP bacteria in the control treatment in the October experiment indicates that this advantage is irrelevant in autumn (Fig.…”

“…However, later observations of their phenology and distribution indicated otherwise: higher concentrations were observed in more eutrophic coastal waters during or shortly after the phytoplankton bloom (Auladell et al ., 2019, Vrdoljak Tomaš et al ., 2019). A similar pattern emerged from freshwater studies (Kolářová et al ., 2019, Villena-Alemany et al ., 2023b), questioning the initial assumption. It was also suggested that additional energy from light can facilitate access to recalcitrant complex organic polymers or low-energy carbon sources, such as lignin or acetate (Koblížek, 2015).…”

“…Subsequent analyses were done in the R/Bioconductor environment using the DADA2 package (version 1.12.1) (Callahan et al ., 2016). puf M sequences were processed and assigned using reference database and methods described in Villena-Alemany et al . (2023b).…”