Seasonal dynamics of aerobic anoxygenic phototrophs in freshwater lake Vlkov

Kolářová, Eva; Medová, Hana; Piwosz, Kasia; Koblížek, Michal

doi:10.1007/s12223-019-00735-x

Cited by 11 publications

(11 citation statements)

References 30 publications

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“…The faster response of AAP bacteria highlights that photoheterotrophy confers a distinct metabolic advantage that triggers their growth in this scenario over other heterotrophic bacteria. Their importance as food for bacterivores in microbial food webs is well documented [95][96][97] and due to their, on average, larger cell size and higher activity than other heterotrophic bacteria [13,14], they contribute disproportionally to the carbon cycling contrary to their relatively low abundances [19,97]. Additionally, Chl-a concentration has been identified as a variable explaining the dynamics of the AAP bacterial community and it is plausible to assume that the spring abundance peaks of AAP bacteria are triggered by the excess of carbon released by the phytoplankton bloom (mostly diatoms; Supplementary Figure S6) and the lack of grazing pressure after winter.…”

Section: Phenology Of Aap Bacteria and Consideration Into The Peg Modelmentioning

confidence: 99%

“…However, little is known on phenology of AAP community and the absence of exhaustive seasonal sampling hampers the understanding of their role in lakes. AAP bacteria peak during spring in lakes, when they may account for up to 22% of bacteria [18,19]. Their abundances and diversity dynamics correlate with irradiance, temperature, chlorophyll-a (Chl-a), oxygen and DOC [18,[20][21][22][23][24].…”

Section: Introductionmentioning

confidence: 99%

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Phenology and ecological role of Aerobic Anoxygenic Phototrophs in fresh waters

Villena-Alemany,

Mujakić,

Fecskeová

et al. 2023

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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.

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Section: Phenology Of Aap Bacteria and Consideration Into The Peg Modelmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Phenology and ecological role of Aerobic Anoxygenic Phototrophs in fresh waters

Villena-Alemany,

Mujakić,

Fecskeová

et al. 2023

Preprint

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“…For example, the Limnohabitans and Polynucleobacter lineages contain numerous AAP bacterial species (30,31). In addition, seasonal maximum abundance of AAP bacteria follows that of phytoplankton blooms in freshwater lakes (32,33). These observations suggest that AAP bacteria can represent a key functional bacterial group whose activity is strongly linked to primary production.…”

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confidence: 96%

Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment

Piwosz

Vrdoljak

Frenken

et al. 2020

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Phytoplankton is a key component of aquatic microbial communities, and metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon (DOC). Yet, the impact of primary production on bacterial activity and community composition remains largely unknown, as, for example, in the case of aerobic anoxygenic phototrophic (AAP) bacteria that utilize both phytoplankton-derived DOC and light as energy sources. Here, we studied how reduction of primary production in a natural freshwater community affects the bacterial community composition and its activity, focusing primarily on AAP bacteria. The bacterial respiration rate was the lowest when photosynthesis was reduced by direct inhibition of photosystem II and the highest in ambient light condition with no photosynthesis inhibition, suggesting that it was limited by carbon availability. However, bacterial assimilation rates of leucine and glucose were unaffected, indicating that increased bacterial growth efficiency (e.g., due to photoheterotrophy) can help to maintain overall bacterial production when low primary production limits DOC availability. Bacterial community composition was tightly linked to light intensity, mainly due to the increased relative abundance of light-dependent AAP bacteria. This notion shows that changes in bacterial community composition are not necessarily reflected by changes in bacterial production or growth and vice versa. Moreover, we demonstrated for the first time that light can directly affect bacterial community composition, a topic which has been neglected in studies of phytoplankton-bacteria interactions. IMPORTANCE Metabolic coupling between phytoplankton and bacteria determines the fate of dissolved organic carbon in aquatic environments, and yet how changes in the rate of primary production affect the bacterial activity and community composition remains understudied. Here, we experimentally limited the rate of primary production either by lowering light intensity or by adding a photosynthesis inhibitor. The induced decrease had a greater influence on bacterial respiration than on bacterial production and growth rate, especially at an optimal light intensity. This suggests that changes in primary production drive bacterial activity, but the effect on carbon flow may be mitigated by increased bacterial growth efficiencies, especially of light-dependent AAP bacteria. Bacterial activities were independent of changes in bacterial community composition, which were driven by light availability and AAP bacteria. This direct effect of light on composition of bacterial communities has not been documented previously.

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“…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).…”

Section: Discussionmentioning

confidence: 86%

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

Piwosz,

Villena-Alemany,

Całkiewicz

et al. 2023

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FigureAerobic Anoxygenic Phototrophic (AAP) bacteria are an important component of freshwater bacterioplankton. They can support their heterotrophic metabolism with energy from light, and by that enhance their growth efficiency. Based on results from cultures, it was hypothesized that photoheterotrophy provides an advantage under carbon limitation and facilitates access to recalcitrant or low-energy carbon sources. However, verification of these hypotheses for natural AAP communities has been lacking. Here, we conducted whole community manipulation experiments and compared the growth of AAP bacteria under carbon limited and with recalcitrant or low-energy carbon sources under dark and light conditions to elucidate how they profit from photoheterotrophy. We found that it depends on the season. In spring, AAP bacteria induce photoheterotrophic metabolism under carbon limitation but they outperform heterotrophic bacteria when carbon is available. This effect seems to be driven by physiological responses rather than changes at the community level. In autumn photoheterotrophy is less beneficial. In both seasons, AAP bacteria responded negatively to recalcitrant or low-energy carbon sources in light. This unexpected observation may have ecosystem-level consequences as lake browning continues. In general, our findings contribute to the understanding of the dynamics of AAP bacteria observed in pelagic environments.

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Seasonal dynamics of aerobic anoxygenic phototrophs in freshwater lake Vlkov

Cited by 11 publications

References 30 publications

Phenology and ecological role of Aerobic Anoxygenic Phototrophs in fresh waters

Phenology and ecological role of Aerobic Anoxygenic Phototrophs in fresh waters

Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment

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

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