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.

Department of Ecosystem Biology Faculty of Science University of South Bohemia 370 05 České Budějovice Czechia

Department of Fisheries Oceanography and Marine Ecology National Marine Fisheries Research Institute 81 332 Gdynia Poland

Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Institute of Aquaculture and Protection of Waters University of South Bohemia 389 25 České Budějovice Czechia

Laboratory of Anoxygenic Phototrophs Institute of Microbiology of the Czech Academy of Sciences 379 01 Třeboň Czechia

Zobrazit více v PubMed

Auladell  A, Sánchez  P, Sánchez  O  et al.  Long-term seasonal and interannual variability of marine aerobic anoxygenic photoheterotrophic bacteria. ISME J. 2019;13:1975–87. 10.1038/s41396-019-0401-4. PubMed DOI PMC

Bugg  TDH, Ahmad  M, Hardiman  EM  et al.  Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep. 2011;28:1883–96. 10.1039/C1NP00042J. PubMed DOI

Callahan  BJ, McMurdie  PJ, Rosen  MJ  et al.  DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3. 10.1038/nmeth.3869. PubMed DOI PMC

Cepáková  Z, Hrouzek  P, Žišková  E  et al.  High turnover rates of aerobic anoxygenic phototrophs in European freshwater lakes. Environ Microbiol. 2016;18:5063–71. 10.1111/1462-2920.13475. PubMed DOI

Coleman  AW. Enhanced detection of bacteria in natural environments by fluorochrome staining of DNA. Limnol Oceanogr. 1980;25:948–51. 10.4319/lo.1980.25.5.0948. DOI

Cottrell  MT, Mannino  A, Kirchman  DL. Aerobic anoxygenic phototrophic bacteria in the Mid-Atlantic Bight and the North Pacific Gyre. Appl Environ Microb. 2006;72:557–64. 10.1128/AEM.72.1.557-564.2006. PubMed DOI PMC

Čuperová  Z, Holzer  E, Salka  I  et al.  Temporal changes and altitudinal distribution of aerobic anoxygenic phototrophs in mountain lakes. Appl Environ Microb. 2013;79:6439–46. 10.1128/aem.01526-13. PubMed DOI PMC

Fauteux  L, Cottrell  MT, Kirchman  DL  et al.  Patterns in abundance, cell size and pigment content of aerobic anoxygenic phototrophic bacteria along environmental gradients in northern lakes. PLoS One. 2015;10:e0124035. 10.1371/journal.pone.0124035. PubMed DOI PMC

Fecskeová  LK, Piwosz  K, Hanusová  M  et al.  Diel changes and diversity of pufM expression in freshwater communities of anoxygenic phototrophic bacteria. Sci Rep. 2019;9:18766. 10.1038/s41598-019-55210-x. PubMed DOI PMC

Fecskeová  LK, Piwosz  K, Šantić  D  et al.  Lineage-specific growth curves document large differences in response of individual groups of marine bacteria to the top-down and bottom-up controls. Msystems. 2021;6:e00934–00921. 10.1128/mSystems.00934-21. PubMed DOI PMC

Garcia-Chaves  MC, Cottrell  MT, Kirchman  DL  et al.  Single-cell activity of freshwater aerobic anoxygenic phototrophic bacteria and their contribution to biomass production. ISME J. 2016;10:1579–88. 10.1038/ismej.2015.242. PubMed DOI PMC

Gómez-Consarnau  L, Raven  JA, Levine  NM  et al.  Microbial rhodopsins are major contributors to the solar energy captured in the sea. Sci Adv. 2019;5:eaaw8855. 10.1126/sciadv.aaw8855. PubMed DOI PMC

Griffiths  RI, Whiteley  AS, O'Donnell  AG  et al.  Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microb. 2000;66:5488–91. 10.1128/aem.66.12.5488-5491.2000. PubMed DOI PMC

Hahn  MW, Lunsdorf  H, Wu  QL  et al.  Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia. Appl Environ Microb. 2003;69:1442–51. 10.1128/aem.69.3.1442-1451.2003. PubMed DOI PMC

Hauruseu  D, Koblížek  M.  Influence of light on carbon utilization in aerobic anoxygenic phototrophs. Appl Environ Microb. 2012;78:7414–9. 10.1128/aem.01747-12. PubMed DOI PMC

Kasalický  V, Zeng  Y, Piwosz  K  et al.  Aerobic anoxygenic photosynthesis is commonly present within the genus Limnohabitans. Appl Environ Microb. 2018;84:e02116–02117. 10.1128/aem.02116-17. PubMed DOI PMC

Koblížek  M, Dachev  M, Bína  D  et al.  Utilization of light energy in phototrophic Gemmatimonadetes. J Photochem Photobiol B: Biol. 2020;213:112085. 10.1016/j.jphotobiol.2020.112085. PubMed DOI

Koblížek  M, Masin  M, Ras  J  et al.  Rapid growth rates of aerobic anoxygenic phototrophs in the ocean. Environ Microbiol. 2007;9:2401–6. 10.1111/j.1462-2920.2007.01354.x. PubMed DOI

Koblížek  M, Mlčoušková  J, Kolber  Z  et al.  On the photosynthetic properties of marine bacterium COL2P belonging to Roseobacter clade. Arch Microbiol. 2010;192:41–9. 10.1007/s00203-009-0529-0. PubMed DOI

Koblížek  M. Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiol Rev. 2015;39:854–70. 10.1093/femsre/fuv032. PubMed DOI

Kolářová  E, Medová  H, Piwosz  K  et al.  Seasonal dynamics of aerobic anoxygenic phototrophs in freshwater lake Vlkov. Folia Microbiol. 2019;64:705–10. 10.1007/s12223-019-00735-x. PubMed DOI

Kolber  ZS, Plumley  FG, Lang  AS  et al.  Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science. 2001;292:2492–5. 10.1126/science.1059707. PubMed DOI

Kopejtka  K, Tomasch  J, Zeng  Y  et al.  Simultaneous presence of Bacteriochlorophyll and Xanthorhodopsin genes in a freshwater bacterium. Msystems. 2020;5:e01044–01020. 10.1128/mSystems.01044-20. PubMed DOI PMC

Kopejtka  K, Zeng  Y, Kaftan  D  et al.  Characterization of the aerobic anoxygenic phototrophic bacterium Sphingomonas sp. AAP5. Microorganisms. 2021;9:768. 10.3390/microorganisms9040768. PubMed DOI PMC

Kritzberg  ES, Hasselquist  EM, Škerlep  M  et al.  Browning of freshwaters: consequences to ecosystem services, underlying drivers, and potential mitigation measures. Ambio. 2020;49:375–90. 10.1007/s13280-019-01227-5. PubMed DOI PMC

Kuzyk  SB, Messner  K, Plouffe  J  et al.  Diverse aerobic anoxygenic phototrophs synthesize bacteriochlorophyll in oligotrophic rather than copiotrophic conditions, suggesting ecological niche. Environ Microbiol. 2023;25:2653–65. 10.1111/1462-2920.16482. PubMed DOI

Lew  S, Koblížek  M, Lew  M  et al.  Seasonal changes of microbial communities in two shallow peat bog lakes. Folia Microbiol. 2015;60:165–75. 10.1007/s12223-014-0352-0. PubMed DOI

Lin  H, Peddada  SD. Analysis of compositions of microbiomes with bias correction. Nat Commun. 2020;11:3514. 10.1038/s41467-020-17041-7. PubMed DOI PMC

Martin  M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal. 2011;17:10–2. 10.14806/ej.17.1.200. DOI

Masin  M, Cuperova  Z, Hojerova  E  et al.  Distribution of aerobic anoxygenic phototrophic bacteria in glacial lakes of northern Europe. Aquat Microb Ecol. 2012;66:77–86. 10.3354/ame01558. DOI

Masin  M, Nedoma  J, Pechar  L  et al.  Distribution of aerobic anoxygenic phototrophs in temperate freshwater systems. Environ Microbiol. 2008;10:1988–96. 10.1111/j.1462-2920.2008.01615.x. PubMed DOI

McMurdie  PJ, Holmes  S. Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comp Biol. 2014;10:e1003531. 10.1371/journal.pcbi.1003531. PubMed DOI PMC

Meyer-Jacob  C, Michelutti  N, Paterson  AM  et al.  The browning and re-browning of lakes: divergent lake-water organic carbon trends linked to acid deposition and climate change. Sci Rep. 2019;9:16676. 10.1038/s41598-019-52912-0. PubMed DOI PMC

Nercessian  O, Noyes  E, Kalyuzhnaya  MG  et al.  Bacterial populations active in metabolism of C-1 compounds in the sediment of Lake Washington, a freshwater lake. Appl Environ Microb. 2005;71:6885–99. 10.1128/aem.71.11.6885-6899.2005. PubMed DOI PMC

Okamura  K, Mitsumori  F, Ito  O  et al.  Photophosphorylation and oxidative phosphorylation in intact cells and chromatophores of an aerobic photosynthetic bacterium, Erythrobacter sp. strain OCh114. J Bacteriol. 1986;168:1142–6. 10.1128/jb.168.3.1142-1146.1986. PubMed DOI PMC

Piwosz  K, Kaftan  D, Dean  J  et al.  Non-linear effect of irradiance on photoheterotrophic activity and growth of the aerobic anoxygenic phototrophic bacterium Dinoroseobacter shibae. Environ Microbiol. 2018a;20:724–33. 10.1111/1462-2920.14003. PubMed DOI

Piwosz  K, Całkiewicz  J, Gołębiewski  M  et al.  Diversity and community composition of pico- and nanoplanktonic protists in the Vistula River estuary (Gulf of Gdańsk, Baltic Sea). Estuar Coast Shelf Sci. 2018b;207:242–9. 10.1016/j.ecss.2018.04.013. DOI

Piwosz  K, Villena-Alemany  C, Mujakić  I.  Photoheterotrophy by aerobic anoxygenic bacteria modulates carbon fluxes in a freshwater lake. ISME J. 2022;16:1046–54. 10.1038/s41396-021-01142-2. PubMed DOI PMC

Piwosz  K, Vrdoljak  A, Frenken  T  et al.  Light and primary production shape bacterial activity and community composition of aerobic anoxygenic phototrophic bacteria in a microcosm experiment. mSphere. 2020;5:e00354–00320. 10.1128/mSphere.00354-20. PubMed DOI PMC

Piwosz  K. Response of aerobic anoxygenic phototrophic bacteria to carbon limitation. Dataset, PANGAEA, 2024. 10.1594/PANGAEA.967435. PubMed DOI PMC

Ruiz-González  C, Garcia-Chaves  MC, Ferrera  I  et al.  Taxonomic differences shape the responses of freshwater aerobic anoxygenic phototrophic bacterial communities to light and predation. Mol Ecol. 2020;29:1267–83. 10.1111/mec.15404. PubMed DOI

Salka  I, Srivastava  A, Allgaier  M  et al.  The draft genome sequence of Sphingomonas sp. strain FukuSWIS1, obtained from acidic lake Grosse Fuchskuhle, indicates photoheterotrophy and a potential for humic matter degradation. Genome Announc. 2014;2:e01183–01114. 10.1128/genomeA.01183-14. PubMed DOI PMC

Shabarova  T, Salcher  MM, Porcal  P  et al.  Recovery of freshwater microbial communities after extreme rain events is mediated by cyclic succession. Nat Microbiol. 2021;6:479–88. 10.1038/s41564-020-00852-1. PubMed DOI

Shiba  T, Shioi  Y, Takamiya  K-I  et al.  Distribution and physiology of aerobic bacteria containing Bacteriochlorophyll a on the east and west coasts of Australia. Appl Environ Microb. 1991;57:295–300. 10.1128/aem.57.1.295-300.1991. PubMed DOI PMC

Shiba  T, Simidu  U, Taga  N. Distribution of aerobic bacteria which contain Bacteriochlorophyll a. Appl Environ Microb. 1979;38:43–5. 10.1128/aem.38.1.43-45.1979. PubMed DOI PMC

Šimek  K, Grujčić  V, Mukherjee  I  et al.  Cascading effects in freshwater microbial food webs by predatory Cercozoa, Katablepharidacea and ciliates feeding on aplastidic bacterivorous cryptophytes. FEMS Microbiol Ecol. 2020;96:fiaa121. 10.1093/femsec/fiaa121. PubMed DOI PMC

Steinberg  CEW, Kamara  S, Prokhotskaya  VY  et al.  Dissolved humic substances—ecological driving forces from the individual to the ecosystem level?. Freshwat Biol. 2006;51:1189–210. 10.1111/j.1365-2427.2006.01571.x. DOI

The R Core Team . R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2021. http://www.R-project.org/ (31 March 2024, date last accessed).

Villena-Alemany  C, Mujakic  I, Fecskeova  LK  et al.  Phenology and ecological role of aerobic anoxygenic phototrophs in fresh waters. Microbiome. 2024;12:65. 10.1186/s40168-024-01786-0. PubMed DOI PMC

Villena-Alemany  C, Mujakić  I, Porcal  P  et al.  Diversity dynamics of aerobic anoxygenic phototrophic bacteria in a freshwater lake. Environ Microbiol Rep. 2023;15:60–71. 10.1111/1758-2229.13131. PubMed DOI PMC

Vrdoljak Tomaš  A, Šantić  D, Šolić  M  et al.  Dynamics of aerobic anoxygenic phototrophs along the trophic gradient in the central Adriatic Sea. Deep Sea Res Part II. 2019;164:112–21. 10.1016/j.dsr2.2019.06.001. DOI

Willems  A, Busse  J, Goor  M  et al.  Hydrogenophaga, a new genus of hydrogen-oxidizing bacteria that includes Hydrogenophaga flava comb. nov. (formerly Pseudomonas flava), Hydrogenophaga palleronii (formerly Pseudomonas palleronii), Hydrogenophaga pseudoflava (formerly Pseudomonas pseudoflava and “Pseudomonas carboxydoflava”), and Hydrogenophaga taeniospiralis (formerly Pseudomonas taeniospiralis). Int J Syst Evol Microbiol. 1989;39:319–33. 10.1099/00207713-39-3-319. DOI

Williamson  CE, Overholt  EP, Pilla  RM  et al.  Ecological consequences of long-term browning in lakes. Sci Rep. 2015;5:18666. 10.1038/srep18666. PubMed DOI PMC

Yurkov  V, Gorlenko  VM.  Erythrobacter sibiricus sp. nov., a new freshwater aerobic bacterial species containing bacteriochlorophyll a. Microbiology. 1990;59:85–9.

Yurkov  VV, Beatty  JT. Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev. 1998;62:695–724. PubMed PMC

Yurkov  VV, Van Gemerden  H.  Impact of light/dark regimen on growth rate, biomass formation and bacteriochlorophyll synthesis in Erythromicrobium hydrolyticum. Arch Microbiol. 1993;159:84–9. 10.1007/bf00244268. DOI

Yutin  N, Suzuki  MT, Béjà  O. Novel primers reveal wider diversity among marine aerobic anoxygenic phototrophs. Appl Environ Microb. 2005;71:8958–62. 10.1128/aem.71.12.8958-8962.2005. PubMed DOI PMC

Response of aerobic anoxygenic phototrophic bacteria to limitation and availability of organic carbon