Aerobic anoxygenic phototrophic (AAP) bacteria are an important component of freshwater bacterioplankton. They can support their heterotrophic metabolism with energy from light, enhancing 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 (near-infrared light, λ > 800 nm) conditions to elucidate how they profit from photoheterotrophy. We found that AAP bacteria induce photoheterotrophic metabolism under carbon limitation, but they overcompete heterotrophic bacteria when carbon is available. This effect seems to be driven by physiological responses rather than changes at the community level. Interestingly, recalcitrant (lignin) or low-energy (acetate) carbon sources inhibited the growth of AAP bacteria, especially 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 in pelagic environments.

• Keywords
• acetate, aerobic anoxygenic phototrophic bacteria, carbon limitation, freshwater lakes, lignin, microbial ecology,
• MeSH
• Bacteria, Aerobic metabolism   growth & development   MeSH
• Bacteria metabolism   growth & development   genetics   MeSH
• Ecosystem MeSH
• Phototrophic Processes * MeSH
• Heterotrophic Processes MeSH
• Lakes microbiology   MeSH
• Light MeSH
• Carbon * metabolism   MeSH
• Publication type
• Journal Article MeSH
• Names of Substances
• Carbon * MeSH

Aerobic anoxygenic photoheterotrophic (AAP) bacteria represent a functional group of prokaryotic organisms that harvests light energy using bacteriochlorophyll-containing photosynthetic reaction centers. They represent an active and rapidly growing component of freshwater bacterioplankton, with the highest numbers observed usually in summer. Species diversity of freshwater AAP bacteria has been studied before in lakes, but its seasonal dynamics remain unknown. In this report, we analysed temporal changes in the composition of the phototrophic community in an oligo-mesotrophic freshwater lake using amplicon sequencing of the pufM marker gene. The AAP community was dominated by phototrophic Gammaproteobacteria and Alphaproteobacteria, with smaller contribution of phototrophic Chloroflexota and Gemmatimonadota. Phototrophic Eremiobacteriota or members of Myxococcota were not detected. Interestingly, some AAP taxa, such as Limnohabitans, Rhodoferax, Rhodobacterales or Rhizobiales, were permanently present over the sampling period, while others, such as Sphingomonadales, Rhodospirillales or Caulobacterales appeared only transiently. The environmental factors that best explain the seasonal changes in AAP community were temperature, concentrations of oxygen and dissolved organic matter.

• MeSH
• Bacteria, Aerobic genetics   MeSH
• Alphaproteobacteria * genetics   MeSH
• Phototrophic Processes MeSH
• Gammaproteobacteria * MeSH
• Lakes microbiology   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH

Photoheterotrophic bacteria harvest light energy using either proton-pumping rhodopsins or bacteriochlorophyll (BChl)-based photosystems. The bacterium Sphingomonas glacialis AAP5 isolated from the alpine lake Gossenköllesee contains genes for both systems. Here, we show that BChl is expressed between 4°C and 22°C in the dark, whereas xanthorhodopsin is expressed only at temperatures below 16°C and in the presence of light. Thus, cells grown at low temperatures under a natural light-dark cycle contain both BChl-based photosystems and xanthorhodopsins with a nostoxanthin antenna. Flash photolysis measurements proved that both systems are photochemically active. The captured light energy is used for ATP synthesis and stimulates growth. Thus, S. glacialis AAP5 represents a chlorophototrophic and a retinalophototrophic organism. Our analyses suggest that simple xanthorhodopsin may be preferred by the cells under higher light and low temperatures, whereas larger BChl-based photosystems may perform better at lower light intensities. This indicates that the use of two systems for light harvesting may represent an evolutionary adaptation to the specific environmental conditions found in alpine lakes and other analogous ecosystems, allowing bacteria to alternate their light-harvesting machinery in response to large seasonal changes of irradiance and temperature.

• Keywords
• anoxygenic photosynthesis, bacteriochlorophyll a, dual phototrophy, light energy, xanthorhodopsin,
• MeSH
• Bacteria metabolism   MeSH
• Bacterial Proteins metabolism   MeSH
• Bacteriochlorophylls * chemistry   MeSH
• Ecosystem MeSH
• Photosynthesis MeSH
• Lakes * analysis   MeSH
• Proton Pumps MeSH
• Protons MeSH
• Light-Harvesting Protein Complexes metabolism   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Bacterial Proteins MeSH
• Bacteriochlorophylls * MeSH
• Proton Pumps MeSH
• Protons MeSH
• Light-Harvesting Protein Complexes MeSH