Aerobic anoxygenic phototrophs (AAPs) are bacteriochlorophyll a-containing microorganisms that use organic substrates for growth but can supplement their energy requirements with light. They have been reported from various marine and limnic environments; however, their ecology remains largely unknown. Here infrared epifluorescence microscopy was used to monitor temporal changes in AAPs in the alpine lake Gossenköllesee, located in the Tyrolean Alps, Austria. AAP abundance was low (10(3) cells ml(-1)) until mid-July and reached a maximum of ∼1.3 × 10(5) cells ml(-1) (29% of all prokaryotes) in mid-September. We compared the studied lake with other mountain lakes located across an altitudinal gradient (913 to 2,799 m above sea level). The concentration of dissolved organic carbon and water transparency seem to be the main factors influencing AAP abundance during the seasonal cycle as well as across the altitudinal gradient. While the AAP populations inhabiting the alpine lakes were composed of intensely pigmented large rods (5 to 12 μm), the lakes below the tree line were inhabited by a variety of smaller morphotypes. Analysis of pufM diversity revealed that AAPs in Gossenköllesee were almost exclusively Sphingomonadales species, which indicates that AAP communities inhabiting alpine lakes are relatively homogeneous compared to those in low-altitude lakes.

Institute of Microbiology CAS Opatovický mlýn Třeboň Czech Republic

See more in PubMed

Koblížek M. 2011. Role of photoheterotrophic bacteria in the marine carbon cycle, p 49–51 In Jiao N, Azam F, Sanders S. (ed), Microbial carbon pump in the ocean. Science/AAAS, Washington, DC

Yurkov VV, Csotonyi JT. 2009. New light on aerobic anoxygenic phototrophs, p 31–55 In Hunter CN, Daldal F, Thurnauer MC, Beatty JT. (ed), The purple phototrophic bacteria, vol. 28. Advances in photosynthesis and respiration. Springer Verlag, New York, NY

Hauruseu D, Koblížek M. 2012. The influence of light on carbon utilization in aerobic anoxygenic phototrophs. Appl. Environ. Microbiol. 78:7414–7419 PubMed PMC

Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani C, Koblížek M, Rathgeber C, Falkowski PG. 2001. Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292:2492–2495 PubMed

Sieracki ME, Gilg IC, Thier EC, Poulton NJ, Goericke R. 2006. Distribution of planktonic aerobic anoxygenic photoheterotrophic bacteria in the northwest Atlantic. Limnol. Oceanogr. 51:38–46

Jiao N, Zhang Y, Zeng Y, Hong N, Liu R, Chen F, Wang P. 2007. Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean. Environ. Microbiol. 9:3091–3099 PubMed

Mašín M, Zdun A, Stoń-Eigert J, Nausch M, Labrenz M, Moulisová V, Koblížek M. 2006. Seasonal changes and diversity of aerobic anoxygenic phototrophs in the Baltic Sea. Aquat. Microb. Ecol. 45:247–254

Cottrell MT, Ras J, Kirchmann DL. 2010. Bacteriochlorophyll and community structure of aerobic anoxygenic phototrophic bacteria in a particle-rich estuary. ISME J. 4:945–954 PubMed

Béjà O, Suzuki MT, Heidelberg JF, Nelson WC, Preston CM, Hamada T, Eisen JA, Fraser CM, DeLong EF. 2002. Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature 415:630–633 PubMed

Yutin N, Suzuki MT, Teeling H, Weber M, Venter JC, Rusch DB, Béjà O. 2007. Assessing diversity and biogeography of aerobic anoxygenic phototrophic bacteria in surface waters of the Atlantic and Pacific Oceans using the Global Ocean Sampling expedition metagenomes. Environ. Microbiol. 9:1464–1475 PubMed

Yurkov VV, Gorlenko VM. 1990. Erythrobacter sibiricus sp. nov., a new freshwater aerobic species containing bacteriochlorophyll a. Mikrobiologiia 59:120–126

Yurkov VV, Gorlenko VM. 1992. New species of aerobic bacteria from the genus Erythromicrobium containing bacteriochlorophyll a. Mikrobiologiia 61:248–255

Fuerst JA, Hawkins JA, Holmes A, Sly LI, Moore CJ, Stackebrandt E. 1993. Porphyrobacter neustonensis gen. nov., sp. nov., an aerobic bacteriochlorophyll-synthesizing budding bacterium from fresh water. Int. J. Syst. Bacteriol. 43:125–134 PubMed

Suyama T, Shigematsu T, Takaichi S, Nodasaka Y, Fujikawa S, Hosoya H, Tokia Y, Kanagawa T, Hanada S. 1999. Roseateles depolymerans gen. nov., sp. nov., a new bacteriochlorophyll a-containing obligate aerobe belonging to the β-subclass of the Proteobacteria. Int. J. Syst. Bacteriol. 49:449–457 PubMed

Page KA, Connon SA, Giovannoni SJ. 2004. Representative freshwater bacterioplankton isolated from Crater Lake, Oregon. Appl. Environ. Microbiol. 70:6542–6550 PubMed PMC

Gich F, Overmann J. 2006. Sandarakinorhabdus limnophila gen. nov., sp. nov., a novel bacteriochlorophyll α-containing, obligately aerobic bacterium isolated from freshwater lakes. Int. J. Syst. Evol. Microbiol. 56:847–854 PubMed

Waidner LA, Kirchman DL. 2005. Aerobic anoxygenic photosynthesis genes and operons in uncultured bacteria in the Delaware River. Environ. Microbiol. 7:1896–1908 PubMed

Eiler A, Beier S, Sawstrom C, Karlsson J, Bertilsson S. 2009. High ratio of bacteriochlorophyll biosynthesis genes to chlorophyll biosynthesis genes in bacteria of humic lakes. Appl. Environ. Microbiol. 75:7221–7228 PubMed PMC

Salka I, Čuperová Z, Mašín M, Koblížek M, Grossart HP. 2011. Rhodoferax-related pufM gene cluster dominates the aerobic anoxygenic phototrophic communities in German freshwater lakes. Environ. Microbiol. 13:2865–2875 PubMed

Martinez-Garcia M, Swan BK, Poulton NJ, Gomez ML, Masland D, Sieracki ME, Stepanauskas R. 2012. High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton. ISME J. 6:113–123 PubMed PMC

Mašín M, Nedoma J, Pechar L, Koblížek M. 2008. Distribution of aerobic anoxygenic phototrophs in temperate freshwater systems. Environ. Microbiol. 10:1988–1996 PubMed

Mašín M, Čuperová Z, Hojerová E, Salka I, Grossart HP, Koblížek M. 2012. Distribution of aerobic anoxygenic phototrophic bacteria in glacial lakes of northern Europe. Aquat. Microb. Ecol. 66:77–86

Sommaruga R. 2001. The role of solar UV radiation in the ecology of alpine lakes. J. Photochem. Photobiol. B 62:35–42 PubMed

Rose KC, Williamson CE, Saros JE, Sommaruga R, Fischer JM. 2009. Differences in UV transparency and thermal structure between alpine and subalpine lakes: implications for organisms. Photochem. Photobiol. Sci. 8:1244–1256 PubMed PMC

Laurion I, Ventura M, Catalan J, Psenner R, Sommaruga R. 2000. Attenuation of ultraviolet radiation in mountain lakes: factors controlling the among- and within-lake variability. Limnol. Oceanogr. 45:1274–1288

Kolber ZS, Van Dover CL, Niedermann RA, Falkowski PG. 2000. Bacterial photosynthesis in surface waters of the open ocean. Nature 407:177–179 PubMed

Sommaruga R, Augustin G. 2006. Seasonality in UV transparency of an alpine lake is associated to changes in phytoplankton biomass. Aquat. Sci. 68:129–141

Catalan J, Ventura M, Brancelj A, Granados I, Thies H, Nickus U, Korhola A, Lotter AF, Barbieri A, Stuchlík E, Lien L, Bitušík P, Buchaca T, Camarero L, Goudsmit GH, Kopáček J, Lemcke G, Livingstone DM, Müller B, Rautio M, Šiško M, Sorvari S, Šporka F, Strunecký O, Toro M. 2002. Seasonal ecosystem variability in remote mountain lakes: implications for detecting climatic signals in sediment records. J. Paleolimnol. 28:25–46

Schmid M, Ambühl H. 1965. Die Bestimmung geringster Mengen von Gesamptphosphor im Wasser von Binnenseen. Schweiz. Z. Hydrol. 27:184–192

Lorenzen CJ. 1967. Determination of chlorophyll and pheopigments: spectrophotometric equations. Limnol. Oceanogr. 12:343–346

Pérez MT, Sommaruga R. 2006. Differential effect of algal- and soil-derived dissolved organic matter on alpine lake bacterial community composition and activity. Limnol. Oceanogr. 51:2527–2537

Pérez MT, Sommaruga R. 2011. Temporal changes in the dominance of major planktonic bacterial groups in an alpine lake: discrepancy with their contribution to bacterial production. Aquat. Microb. Ecol. 63:161–170

Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537–7541 PubMed PMC

ter Braak CJF. 1989. CANOCO—an extension of DECORANA to analyze species-environment relationships. Hydrobiologia 184:169–170

Cottrell MT, Mannino A, Kirchman DL. 2006. Aerobic anoxygenic phototrophic bacteria in the mid-Atlantic bight and the north Pacific gyre. Appl. Environ. Microbiol. 72:557–564 PubMed PMC

Hojerová E, Mašín M, Brunet C, Ferrera I, Gasol JM, Koblížek M. 2011. Distribution and growth of aerobic anoxygenic phototrophs in the Mediterranean Sea. Environ. Microbiol. 13:2717–2725 PubMed

Kosako Y, Yabuuchi E, Naka T, Fujiwara N, Kobayashi K. 2000. Proposal of Spingomonadaceae fam. nov., consisting of Sphingomonas Yabuuchi et al. 1990, Erythrobacter Shiba and Shimidu 1982, Erythromicrobium Yurkov et al. 1994, Porphyrobacter Fuerst et al. 1993, Zymomonas Kluyver and van Niel 1936, and Sandaracinobacter Yurkov et al. 1997, with the type genus Sphingomonas Yabuuchi et al. 1990. Microbiol. Immunol. 44:563–575 PubMed

Waidner LA, Kirchman DL. 2008. Diversity and distribution of ecotypes of the aerobic anoxygenic phototrophy gene pufM in the Delaware estuary. Appl. Environ. Microbiol. 74:4012–4021 PubMed PMC

Hörtnagl P, Pérez MT, Sommaruga R. 2010. Living at the border: a community and single-cell assessment of lake bacterioneuston activity. Limnol. Oceanogr. 55:1134–1144 PubMed PMC

Joux F, Jeffrey WH, Lebaron P, Mitchell DL. 1999. Marine bacterial isolates display diverse responses to UV-B radiation. Appl. Environ. Microbiol. 65:3820–3827 PubMed PMC

Lamy D, De Carvalho-Maalouf P, Cottrell MT, Lami R, Catala P, Oriol L, Caparros J, Ras J, Kirchman DL, Lebaron P. 2011. Seasonal dynamics of aerobic anoxygenic phototrophs in a Mediterranean coastal lagoon. Aquat. Microb. Ecol. 62:153–163

Koblížek M, Ston-Egiert J, Sagan S, Kolber ZS. 2005. Diel changes in bacteriochlorophyll α concentration suggest rapid bacterioplankton cycling in the Baltic Sea. FEMS Microbiol. Ecol. 51:353–361 PubMed

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

Phenology and ecological role of aerobic anoxygenic phototrophs in freshwaters

Diversity dynamics of aerobic anoxygenic phototrophic bacteria in a freshwater lake

A bacterium from a mountain lake harvests light using both proton-pumping xanthorhodopsins and bacteriochlorophyll-based photosystems

Characterization of the Aerobic Anoxygenic Phototrophic Bacterium Sphingomonas sp. AAP5

Simultaneous Presence of Bacteriochlorophyll and Xanthorhodopsin Genes in a Freshwater Bacterium

Diel changes and diversity of pufM expression in freshwater communities of anoxygenic phototrophic bacteria

Seasonal dynamics of aerobic anoxygenic phototrophs in freshwater lake Vlkov

Aerobic Anoxygenic Photosynthesis Is Commonly Present within the Genus Limnohabitans

Novel acsF Gene Primers Revealed a Diverse Phototrophic Bacterial Population, Including Gemmatimonadetes, in Lake Taihu (China)

Influence of selected environmental factors on the abundance of aerobic anoxygenic phototrophs in peat-bog lakes

See more in PubMed

GENBANK
JN715070, JN715071, JN715072, JN715073, JN715074, JN715075, JN715076