Aerobic anoxygenic phototrophic (AAP) bacteria harvest light energy using bacteriochlorophyll-containing reaction centers to supplement their mostly heterotrophic metabolism. While their abundance and growth have been intensively studied in coastal environments, much less is known about their activity in oligotrophic open ocean regions. Therefore, we combined in situ sampling in the North Pacific Subtropical Gyre, north of O'ahu island, Hawaii, with two manipulation experiments. Infra-red epifluorescence microscopy documented that AAP bacteria represented approximately 2% of total bacteria in the euphotic zone with the maximum abundance in the upper 50 m. They conducted active photosynthetic electron transport with maximum rates up to 50 electrons per reaction center per second. The in situ decline of bacteriochlorophyll concentration over the daylight period, an estimate of loss rates due to predation, indicated that the AAP bacteria in the upper 50 m of the water column turned over at rates of 0.75-0.90 d-1. This corresponded well with the specific growth rate determined in dilution experiments where AAP bacteria grew at a rate 1.05 ± 0.09 d-1. An amendment of inorganic nitrogen to obtain N:P = 32 resulted in a more than 10 times increase in AAP abundance over 6 days. The presented data document that AAP bacteria are an active part of the bacterioplankton community in the oligotrophic North Pacific Subtropical Gyre and that their growth was mostly controlled by nitrogen availability and grazing pressure.IMPORTANCEMarine bacteria represent a complex assembly of species with different physiology, metabolism, and substrate preferences. We focus on a specific functional group of marine bacteria called aerobic anoxygenic phototrophs. These photoheterotrophic organisms require organic carbon substrates for growth, but they can also supplement their metabolic needs with light energy captured by bacteriochlorophyll. These bacteria have been intensively studied in coastal regions, but rather less is known about their distribution, growth, and mortality in the oligotrophic open ocean. Therefore, we conducted a suite of measurements in the North Pacific Subtropical Gyre to determine the distribution of these organisms in the water column and their growth and mortality rates. A nutrient amendment experiment showed that aerobic anoxygenic phototrophs were limited by inorganic nitrogen. Despite this, they grew more rapidly than average heterotrophic bacteria, but their growth was balanced by intense grazing pressure.

Centro Oceanográfico de Málaga Instituto Español de Oceanografía Fuengirola Málaga Spain

Department of Cellular and Molecular Biology University of Arizona Tucson Arizona USA

Department of Marine Chemistry and Geochemistry Woods Hole Oceanographic Institution Woods Hole Massachusetts USA

Institut de Ciències del Mar Barcelona Catalonia Spain

Laboratory of Anoxygenic Phototrophs Institute of Microbiology Czech Academy of Science Třeboň Czechia

Rosenstiel School of Marine Atmospheric and Earth Science University of Miami Coral Gables Florida USA

Zobrazit více v PubMed

Koblížek M. 2015. Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiol Rev 39:854–870. doi:10.1093/femsre/fuv032 PubMed DOI

Yurkov VV, Hughes E. 2017. Aerobic anoxygenic phototrophs: four decades of mystery, p 193–214. In Modern topic in the phototrophic prokaryotes. Hallenbeck PC. Springer, Switzerland.

Kolber ZS, Van Dover CL, Niederman RA, Falkowski PG. 2000. Bacterial photosynthesis in surface waters of the open ocean. Nature 407:177–179. doi:10.1038/35025044 PubMed DOI

Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani C, Koblizek M, Rathgeber C, Falkowski PG. 2001. Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292:2492–2495. doi:10.1126/science.1059707 PubMed DOI

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. doi:10.1128/AEM.72.1.557-564.2006 PubMed DOI PMC

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. doi:10.4319/lo.2006.51.1.0038 DOI

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. doi:10.1111/j.1462-2920.2007.01419.x PubMed DOI

Lami R, Cottrell MT, Ras J, Ulloa O, Obernosterer I, Claustre H, Kirchman DL, Lebaron P. 2007. High abundances of aerobic anoxygenic photosynthetic bacteria in the South Pacific ocean. Appl Environ Microbiol 73:4198–4205. doi:10.1128/AEM.02652-06 PubMed DOI PMC

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. doi:10.1038/415630a PubMed DOI

Hu YH, Du HL, Jiao NZ, Zeng Y. 2006. Abundant presence of the gamma-like proteobacterial pufM gene in oxic seawater. FEMS Microbiol Lett 263:200–206. doi:10.1111/j.1574-6968.2006.00421.x PubMed DOI

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. doi:10.1111/j.1462-2920.2007.01265.x PubMed DOI

Jeanthon C, Boeuf D, Dahan O, Le Gall F, Garczarek L, Bendif EM, Lehours A-C. 2011. Diversity of cultivated and metabolically active aerobic anoxygenic phototrophic bacteria along an oligotrophic gradient in the Mediterranean Sea. Biogeosciences 8:1955–1970. doi:10.5194/bg-8-1955-2011 DOI

Ritchie AE, Johnson ZI. 2012. Abundance and genetic diversity of aerobic anoxygenic phototrophic bacteria of coastal regions of the Pacific ocean. Appl Environ Microbiol 78:2858–2866. doi:10.1128/AEM.06268-11 PubMed DOI PMC

Bibiloni-Isaksson J, Seymour JR, Ingleton T, van de Kamp J, Bodrossy L, Brown MV. 2016. Spatial and temporal variability of aerobic anoxygenic photoheterotrophic bacteria along the East coast of Australia. Environ Microbiol 18:4485–4500. doi:10.1111/1462-2920.13436 PubMed DOI

Lehours AC, Enault F, Boeuf D, Jeanthon C. 2018. Biogeographic patterns of aerobic anoxygenic phototrophic bacteria reveal an ecological consistency of phylogenetic clades in different oceanic biomes. Sci Rep 8:4105. doi:10.1038/s41598-018-22413-7 PubMed DOI PMC

Auladell A, Sánchez P, Sánchez O, Gasol JM, Ferrera I. 2019. Long-term seasonal and interannual variability of marine aerobic anoxygenic photoheterotrophic bacteria. ISME J 13:1975–1987. doi:10.1038/s41396-019-0401-4 PubMed DOI PMC

Gazulla CR, Cabello AM, Sánchez P, Gasol JM, Sánchez O, Ferrera I. 2023. A metagenomic and amplicon sequencing combined approach reveals the best primers to study marine aerobic anoxygenic phototrophs. Microb Ecol 86:2161–2172. doi:10.1007/s00248-023-02220-y PubMed DOI PMC

Okamura K, Mitsumori F, Ito O, Takamiya KI, Nishimura M. 1986. Photophosphorylation and oxidative phosphorylation in intact cells and chromatophores of an aerobic photosynthetic bacterium, Erythrobacter sp. strain OCh114. J Bacteriol 168:1142–1146. doi:10.1128/jb.168.3.1142-1146.1986 PubMed DOI PMC

Candela M, Zaccherini E, Zannoni D. 2001. Respiratory electron transport and light-induced energy transduction in membranes from the aerobic photosynthetic bacterium Roseobacter denitrificans. Arch Microbiol 175:168–177. doi:10.1007/s002030100251 PubMed DOI

Harashima K, Kawazoe K, Yoshida I, Kamata H. 1987. Light stimulated aerobic growth of Erythrobacter species OCh 114. Plant Cell Physiol 28:365–374.

Hauruseu D, Koblížek M. 2012. The influence of light on carbon utilization in aerobic anoxygenic phototrophs. Appl Environ Microbiol 78:7414–7419. doi:10.1128/AEM.01747-12 PubMed DOI PMC

Piwosz K, Kaftan D, Dean J, Šetlík J, Koblížek M. 2018. Nonlinear effect of irradiance on photoheterotrophic activity and growth of the aerobic anoxygenic phototrophic bacterium Dinoroseobacter shibae. Environ Microbiol 20:724–733. doi:10.1111/1462-2920.14003 PubMed DOI

Kirchman DL, Hanson TE. 2013. Bioenergetics of photoheterotrophic bacteria in the oceans. Environ Microbiol Rep 5:188–199. doi:10.1111/j.1758-2229.2012.00367.x PubMed DOI

Ferrera I, Sánchez O, Kolářová E, Koblížek M, Gasol JM. 2017. Light enhances the growth rates of natural populations of aerobic anoxygenic phototrophic bacteria. ISME J 11:2391–2393. doi:10.1038/ismej.2017.79 PubMed DOI PMC

Sánchez O, Ferrera I, Mabrito I, Gazulla CR, Sebastián M, Auladell A, Marín-Vindas C, Cardelús C, Sanz-Sáez I, Pernice MC, Marrasé C, Sala MM, Gasol JM. 2020. Seasonal impact of grazing, viral mortality, resource availability and light on the group-specific growth rates of coastal Mediterranean bacterioplankton. Sci Rep 10:19773. doi:10.1038/s41598-020-76590-5 PubMed DOI PMC

Ferrera I, Gasol JM, Sebastián M, Hojerová E, Koblížek M. 2011. Growth rates of aerobic anoxygenic phototrophic bacteria as compared to other bacterioplankton groups in coastal Mediterranean waters. Appl Environ Microbiol 77:7451–7458. doi:10.1128/AEM.00208-11 PubMed DOI PMC

Fecskeová LK, Piwosz K, Šantić D, Šestanović S, Tomaš AV, Hanusová M, Šolić M, Koblížek M. 2021. Lineage-specific growth curves document large differences in response of individual groups of marine bacteria to the top-down and bottom-up controls. mSystems 6:e0093421. doi:10.1128/mSystems.00934-21 PubMed DOI PMC

Karl DM, Lukas R. 1996. The Hawaii Ocean Time-series (HOT) program: background, rationale and field implementation. Deep-Sea Res II: Top Stud Oceanogr 43:129–156. doi:10.1016/0967-0645(96)00005-7 DOI

Bryant JA, Aylward FO, Eppley JM, Karl DM, Church MJ, DeLong EF. 2016. Wind and sunlight shape microbial diversity in surface waters of the North Pacific Subtropical Gyre. ISME J 10:1308–1322. doi:10.1038/ismej.2015.221 PubMed DOI PMC

Frias-Lopez J, Shi Y, Tyson GW, Coleman ML, Schuster SC, Chisholm SW, Delong EF. 2008. Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci U S A 105:3805–3810. doi:10.1073/pnas.0708897105 PubMed DOI PMC

Koblížek M, Mašín M, Ras J, Poulton AJ, Prášil O. 2007. Rapid growth rates of aerobic anoxygenic phototrophs in the ocean. Environ Microbiol 9:2401–2406. doi:10.1111/j.1462-2920.2007.01354.x PubMed DOI

Lamy D, Jeanthon C, Cottrell MT, Kirchman DL, Van Wambeke F, Ras J, Dahan O, Pujo-Pay M, Oriol L, Bariat L, Catala P, Cornet-Barthaux V, Lebaron P. 2011. Ecology of aerobic anoxygenic phototrophic bacteria along an oligotrophic gradient in the Mediterranean Sea. Biogeosciences 8:973–985. doi:10.5194/bg-8-973-2011 DOI

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. doi:10.1111/j.1462-2920.2011.02540.x PubMed DOI

Šantić D, Šestanović S, Vrdoljak A, Šolić M, Kušpilić G, Ninčević Gladan Ž, Koblížek M. 2017. Distribution of aerobic anoxygenic phototrophs in the Eastern Adriatic sea. Mar Environ Res 130:134–141. doi:10.1016/j.marenvres.2017.07.012 PubMed DOI

Gómez-Consarnau L, Raven JA, Levine NM, Cutter LS, Wang D, Seegers B, Arístegui J, Fuhrman JA, Gasol JM, Sañudo-Wilhelmy SA. 2019. Microbial rhodopsins are major contributors to the solar energy captured in the sea. Sci Adv 5:eaaw8855. doi:10.1126/sciadv.aaw8855 PubMed DOI PMC

Koblížek M, Mlčoušková J, Kolber Z, Kopecký J. 2010. On the photosynthetic properties of marine bacterium COL2P belonging to Roseobacter clade. Arch Microbiol 192:41–49. doi:10.1007/s00203-009-0529-0 PubMed DOI

Selyanin V, Hauruseu D, Koblížek M. 2016. The variability of light-harvesting complexes in aerobic anoxygenic phototrophs. Photosynth Res 128:35–43. doi:10.1007/s11120-015-0197-7 PubMed DOI

Koblížek M, Stoń-Egiert J, Sagan S, Kolber ZS. 2005. Diel changes in bacteriochlorophyll a concentration suggest rapid bacterioplankton cycling in the Baltic sea. FEMS Microbiol Ecol 51:353–361. doi:10.1016/j.femsec.2004.09.016 PubMed DOI

Yurkov VV, van Gemerden H. 1993. Impact of light/dark regimen on growth rate, biomass formation and bacteriochlorophyll synthesis in Erythromicrobium hydrolyticum. Arch Microbiol 159:84–89. doi:10.1007/BF00244268 DOI

Tomasch J, Gohl R, Bunk B, Diez MS, Wagner-Döbler I. 2011. Transcriptional response of the photoheterotrophic marine bacterium Dinoroseobacter shibae to changing light regimes. ISME J 5:1957–1968. doi:10.1038/ismej.2011.68 PubMed DOI PMC

Popendorf KJ, Koblížek M, Van Mooy BAS. 2020. Phospholipid turnover rates suggest that bacterial community growth rates in the open ocean are systematically underestimated. Limnol Oceanograp 65:1876–1890. doi:10.1002/lno.11424 DOI

Kirchman DL. 2016. Growth rates of microbes in the oceans. Ann Rev Mar Sci 8:285–309. doi:10.1146/annurev-marine-122414-033938 PubMed DOI

Landry MR, Stukel MR, Selph KE, Goericke R. 2023. Coexisting picoplankton experience different relative grazing pressures across an ocean productivity gradient. Proc Natl Acad Sci U S A 120:e2220771120. doi:10.1073/pnas.2220771120 PubMed DOI PMC

Letelier RM, Björkman KM, Church MJ, Hamilton DS, Mahowald NM, Scanza RA, Schneider N, White AE, Karl DM. 2019. Climate-driven oscillation of phosphorus and iron limitation in the North Pacific Subtropical Gyre. Proc Natl Acad Sci U S A 116:12720–12728. doi:10.1073/pnas.1900789116 PubMed DOI PMC

Duhamel S, Björkman KM, Doggett JK, Karl DM. 2014. Microbial response to enhanced phosphorus cycling in the North Pacific Subtropical Gyre. Mar Ecol Prog Ser 504:43–58. doi:10.3354/meps10757 DOI

Moore CM, Mills MM, Arrigo KR, Berman-Frank I, Bopp L, Boyd PW, Galbraith ED, Geider RJ, Guieu C, Jaccard SL, Jickells TD, La Roche J, Lenton TM, Mahowald NM, Marañón E, Marinov I, Moore JK, Nakatsuka T, Oschlies A, Saito MA, Thingstad TF, Tsuda A, Ulloa O. 2013. Processes and patterns of oceanic nutrient limitation. Nature Geosci 6:701–710. doi:10.1038/ngeo1765 DOI

Sánchez O, Koblížek M, Gasol JM, Ferrera I. 2017. Effects of grazing, phosphorus and light on the growth rates of major bacterioplankton taxa in the coastal NW Mediterranean. Environ Microbiol Rep 9:300–309. doi:10.1111/1758-2229.12535 PubMed DOI

Karl DM, Bidigare RR, Letelier RM. 2001. Long-term changes in plankton community structure and productivity in the North Pacific Subtropical Gyre: the domain shift hypothesis. Deep-Sea Res II: Top Stud Oceanogr 48:1449–1470. doi:10.1016/S0967-0645(00)00149-1 DOI