Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment
Jazyk angličtina Země Spojené státy americké Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
32611696
PubMed Central
PMC7333569
DOI
10.1128/msphere.00354-20
PII: 5/4/e00354-20
Knihovny.cz E-zdroje
- Klíčová slova
- AAP community composition, aerobic anoxygenic phototrophic bacteria, bacterial community composition, phytoplankton-bacteria coupling,
- MeSH
- aerobní bakterie růst a vývoj metabolismus MeSH
- ekosystém * MeSH
- fotosyntéza MeSH
- fototrofní procesy * MeSH
- fyziologie bakterií MeSH
- mikrobiota * MeSH
- mořská voda mikrobiologie MeSH
- sladká voda mikrobiologie MeSH
- světlo MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
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.
Center Algatech Institute of Microbiology Czech Academy of Sciences Třeboň Czechia
Department of Aquatic Ecology Netherlands Institute of Ecology Wageningen The Netherlands
Department of Life and Environmental Sciences Università Politecnica delle Marche Ancona Italy
Department of Natural Sciences University of Agder Kristiansand Norway
Great Lakes Institute for Environmental Research University of Windsor Windsor Ontario Canada
Institute of Biochemistry and Biology Potsdam University Potsdam Germany
Institute of Hydrobiology Biology Centre Czech Academy of Sciences České Budějovice Czechia
Institute of Oceanography and Fisheries Split Croatia
Israel Oceanographic and Limnological Research National Center for Mariculture Eilat Israel
Marine Research Centre Finnish Environment Institute Helsinki Finland
University Institute of Water Research University of Granada Granada Spain
Zobrazit více v PubMed
Brett MT, Bunn SE, Chandra S, Galloway AWE, Guo F, Kainz MJ, Kankaala P, Lau DCP, Moulton TP, Power ME, Rasmussen JB, Taipale SJ, Thorp JH, Wehr JD. 2017. How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems? Freshw Biol 62:833–853. doi:10.1111/fwb.12909. DOI
Guillemette F, McCallister SL, del Giorgio PA. 2016. Selective consumption and metabolic allocation of terrestrial and algal carbon determine allochthony in lake bacteria. ISME J 10:1373–1382. doi:10.1038/ismej.2015.215. PubMed DOI PMC
Hawkes J, Patriarca C, Sjöberg P, Tranvik L, Bergquist J. 2018. Extreme isomeric complexity of dissolved organic matter found across aquatic environments: extreme isomeric complexity of DOM. Limnol Oceanogr 3:21–30. doi:10.1002/lol2.10064. DOI
Koehler B, Wachenfeldt E, Kothawala D, Tranvik L. 2012. Reactivity continuum of dissolved organic carbon decomposition in lake water. J Geophysical Res (Biogeosciences) 117:1024.
Maki K, Kim C, Yoshimizu C, Tayasu I, Miyajima T, Nagata T. 2010. Autochthonous origin of semi-labile dissolved organic carbon in a large monomictic lake (Lake Biwa): carbon stable isotopic evidence. Limnology 11:143–153. doi:10.1007/s10201-009-0299-z. DOI
Toming K, Tuvikene L, Vilbaste S, Agasild H, Viik M, Kisand A, Feldmann T, Martma T, Jones R, Noges T. 2013. Contributions of autochthonous and allochthonous sources to dissolved organic matter in a large, shallow, eutrophic lake with a highly calcareous catchment. Limnol Oceanogr 58:1259–1270. doi:10.4319/lo.2013.58.4.1259. DOI
Fouilland E, Mostajir B. 2010. Revisited phytoplanktonic carbon dependency of heterotrophic bacteria in freshwaters, transitional, coastal and oceanic waters. FEMS Microbiol Ecol 73:419–429. doi:10.1111/j.1574-6941.2010.00896.x. PubMed DOI
Šimek K, Horňák K, Jezbera J, Nedoma J, Znachor P, Hejzlar J, Sed’a J. 2008. Spatio-temporal patterns of bacterioplankton production and community composition related to phytoplankton composition and protistan bacterivory in a dam reservoir. Aquat Microb Ecol 51:249–262. doi:10.3354/ame01193. DOI
Kritzberg ES, Cole JJ, Pace ML, Graneli W, Bade DL. 2004. Autochthonous versus allochthonous carbon sources of bacteria: results from whole-lake C-13 addition experiments. Limnol Oceanogr 49:588–596. doi:10.4319/lo.2004.49.2.0588. DOI
Kritzberg ES, Cole JJ, Pace MM, Graneli W. 2005. Does autochthonous primary production drive variability in bacterial metabolism and growth efficiency in lakes dominated by terrestrial C inputs? Aquat Microb Ecol 38:103–111. doi:10.3354/ame038103. DOI
Bertilsson S, Jones JB. 2003. Supply of dissolved organic matter to aquatic ecosystems: autochthonous sources, p 3–24. In Findlay SEG, Sinsabaugh RL (ed), Aquatic ecosystems. Academic Press, Burlington, VT.
Eiler A, Heinrich F, Bertilsson S. 2012. Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J 6:330–342. doi:10.1038/ismej.2011.113. PubMed DOI PMC
Camarena-Gómez MT, Lipsewers T, Piiparinen J, Eronen-Rasimus E, Perez-Quemaliños D, Hoikkala L, Sobrino C, Spilling K. 2018. Shifts in phytoplankton community structure modify bacterial production, abundance and community composition. Aquat Microb Ecol 81:149–170. doi:10.3354/ame01868. DOI
Šimek K, Nedoma J, Znachor P, Kasalický V, Jezbera J, Horňák K, Sed’a J. 2014. A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring. Limnol Oceanogr 59:1477–1492. doi:10.4319/lo.2014.59.5.1477. DOI
Eckert EM, Salcher MM, Posch T, Eugster B, Pernthaler J. 2012. Rapid successions affect microbial N-acetyl-glucosamine uptake patterns during a lacustrine spring phytoplankton bloom. Environ Microbiol 14:794–806. doi:10.1111/j.1462-2920.2011.02639.x. PubMed DOI
Horňák K, Kasalický V, Šimek K, Grossart HP. 2017. Strain-specific consumption and transformation of alga-derived dissolved organic matter by members of the Limnohabitans-C and Polynucleobacter-B clusters of Betaproteobacteria. Environ Microbiol 19:4519–4535. doi:10.1111/1462-2920.13900. PubMed DOI
Wang H, Zhu R, Zhang X, Li Y, Ni L, Xie P, Shen H. 2019. Abiotic environmental factors override phytoplankton succession in shaping both free-living and attached bacterial communities in a highland lake. AMB Express 9:170. doi:10.1186/s13568-019-0889-z. PubMed DOI PMC
Danger M, Leflaive J, Oumarou C, Ten-Hage L, Lacroix G. 2007. Control of phytoplankton-bacterium interactions by stoichiometric constraints. Oikos 116:1079–1086. doi:10.1111/j.2007.0030-1299.15424.x. DOI
Gurung TB, Urabe J, Nakanishi M. 1999. Regulation of the relationship between phytoplankton Scenedesmus acutus and heterotrophic bacteria by the balance of light and nutrients. Aquat Microb Ecol 17:27–35. doi:10.3354/ame017027. DOI
Mindl B, Sonntag B, Pernthaler J, Vrba J, Psenner R, Posch T. 2005. Effects of phosphorus loading on interactions of algae and bacteria: reinvestigation of the “phytoplankton-bacterium paradox” in a continuous cultivation system. Aquat Microb Ecol 38:203–213. doi:10.3354/ame038203. DOI
Paver SF, Kent AD. 2017. Direct and context-dependent effects of light, temperature, and phytoplankton shape bacterial community composition. Ecosphere 8:e01948. doi:10.1002/ecs2.1948. DOI
Pope CA, Halvorson HM, Findlay RH, Francoeur SN, Kuehn KA. 2020. Light and temperature mediate algal stimulation of heterotrophic activity on decomposing leaf litter. Freshw Biol doi:10.1111/fwb.13465. DOI
Durán-Romero C, Medina-Sánchez JM, Carrillo P. 2020. Uncoupled phytoplankton-bacterioplankton relationship by multiple drivers interacting at different temporal scales in a high-mountain Mediterranean lake. Sci Rep 10:350. doi:10.1038/s41598-020-62863-6. PubMed DOI PMC
Garcia SL, Szekely AJ, Bergvall C, Schattenhofer M, Peura S. 2019. Decreased snow cover stimulates under-ice primary producers but impairs methanotrophic capacity. mSphere 4:e00626-18. doi:10.1128/mSphere.00626-18. PubMed DOI PMC
Yurkov VV, Beatty JT. 1998. Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62:695–724. doi:10.1128/MMBR.62.3.695-724.1998. PubMed DOI PMC
Hauruseu D, Koblížek M. 2012. 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. Non-linear 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
Garcia-Chaves MC, Cottrell MT, Kirchman DL, Ruiz-González C, Del Giorgio PA. 2016. Single-cell activity of freshwater aerobic anoxygenic phototrophic bacteria and their contribution to biomass production. ISME J 10:1579–1588. doi:10.1038/ismej.2015.242. PubMed DOI PMC
Ferrera I, Gasol JM, Sebastian M, Hojerová E, Koblížek M. 2011. Comparison of growth rates of aerobic anoxygenic phototrophic bacteria and other bacterioplankton groups in coastal Mediterranean waters. Appl Environ Microbiol 77:7451–7458. doi:10.1128/AEM.00208-11. PubMed DOI PMC
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. doi:10.1038/ismej.2011.84. PubMed DOI PMC
Kasalický V, Zeng Y, Piwosz K, Šimek K, Kratochvilová H, Koblížek M. 2017. Common presence of aerobic anoxygenic photosynthesis within the genus Limnohabitans. Appl Environ Microbiol 84:e02116-17. doi:10.1128/AEM.02116-17. PubMed DOI PMC
Kolářová E, Medová H, Piwosz K, Koblížek M. 2019. Seasonal dynamics of aerobic anoxygenic phototrophs in freshwater lake Vlkov. Folia Microbiol 64:705–710. doi:10.1007/s12223-019-00735-x. PubMed DOI
Cepáková Z, Hrouzek P, Žišková E, Nuyanzina-Boldareva E, Šorf M, Kozlíková-Zapomělová E, Salka I, Grossart H-P, Koblížek M. 2016. High turnover rates of aerobic anoxygenic phototrophs in European freshwater lakes. Environ Microbiol 18:5063–5071. doi:10.1111/1462-2920.13475. PubMed DOI
González-Olalla JM, Medina-Sánchez JM, Lozano IL, Villar-Argaiz M, Carrillo P. 2018. Climate-driven shifts in algal-bacterial interaction of high-mountain lakes in two years spanning a decade. Sci Rep 8:10278. doi:10.1038/s41598-018-28543-2. PubMed DOI PMC
Grossart H-P, Czub G, Simon M. 2006. Algae-bacteria interactions and their effects on aggregation and organic matter flux in the sea. Environ Microbiol 8:1074–1084. doi:10.1111/j.1462-2920.2006.00999.x. PubMed DOI
Grossart H-P. 1999. Interactions between marine bacteria and axenic diatoms (Cylindrotheca fusiformis, Nitzschia laevis, and Thalassiosira weissflogii) incubated under various conditions in the lab. Aquat Microb Ecol 19:1–11. doi:10.3354/ame019001. DOI
Hosler JP, Yocum CF. 1987. Regulation of cyclic photophosphorylation during ferredoxin-mediated electron transport. Plant Physiol 83:965–969. doi:10.1104/pp.83.4.965. PubMed DOI PMC
Nedoma J, Porcalová P, Komárková J, Vyhnálek V. 1993. A seasonal study of phosphorus deficiency in a eutrophic reservoir. Freshwater Biol 30:369–376. doi:10.1111/j.1365-2427.1993.tb00821.x. DOI
Znachor P, Zapomělová E, Řeháková K, Nedoma J, Šimek K. 2008. The effect of extreme rainfall on summer succession and vertical distribution of phytoplankton in a lacustrine part of a eutrophic reservoir. Aquat Sci 70:77–86. doi:10.1007/s00027-007-7033-x. DOI
Thingstad TF, Bellerby RGJ, Bratbak G, Børsheim KY, Egge JK, Heldal M, Larsen A, Neill C, Nejstgaard J, Norland S, Sandaa RA, Skjoldal EF, Tanaka T, Thyrhaug R, Töpper B. 2008. Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature 455:387–390. doi:10.1038/nature07235. 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
Šimek K, Weinbauer MG, Horňák K, Jezbera J, Nedoma J, Dolan JR. 2007. Grazer and virus-induced mortality of bacterioplankton accelerates development of Flectobacillus populations in a freshwater community. Environ Microbiol 9:789–800. doi:10.1111/j.1462-2920.2006.01201.x. PubMed DOI
Horňák K, Jezbera J, Nedoma J, Gasol JM, Šimek K. 2006. Effects of resource availability and bacterivory on leucine incorporation in different groups of freshwater bacterioplankton, assessed using microautoradiography. Aquat Microb Ecol 45:277–289. doi:10.3354/ame045277. DOI
Fecskeová LK, Piwosz K, Hanusová M, Nedoma J, Znachor P, Koblížek M. 2019. Diel changes and diversity of pufM expression in freshwater communities of anoxygenic phototrophic bacteria. Sci Rep 9:18766. doi:10.1038/s41598-019-55210-x. PubMed DOI PMC
Shabarova T, Kasalický V, Šimek K, Nedoma J, Znachor P, Posch T, Pernthaler J, Salcher MM. 2017. Distribution and ecological preferences of the freshwater lineage LimA (genus Limnohabitans) revealed by a new double hybridization approach. Environ Microbiol 19:1296–1309. doi:10.1111/1462-2920.13663. PubMed DOI
Ruiz-González C, Simo R, Sommaruga R, Gasol JM. 2013. Away from darkness: a review on the effects of solar radiation on heterotrophic bacterioplankton activity. Front Microbiol 4:131. doi:10.3389/fmicb.2013.00131. PubMed DOI PMC
Znachor P, Nedoma J, Hejzlar J, Seďa J, Kopáček J, Boukal D, Mrkvička T. 2018. Multiple long-term trends and trend reversals dominate environmental conditions in a man-made freshwater reservoir. Sci Total Environ 624:24–33. doi:10.1016/j.scitotenv.2017.12.061. PubMed DOI
Sinning I. 1992. Herbicide binding in the bacterial photosynthetic reaction center. Trends Biochem Sci 17:150–154. doi:10.1016/0968-0004(92)90324-3. PubMed DOI
Lund JWG, Kipling C, Le Cren ED. 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11:143–170. doi:10.1007/BF00007865. DOI
Peterson BJ. 1980. Aquatic primary productivity and the 14C-CO2 method: a history of the productivity problem. Annu Rev Ecol Syst 11:359–385. doi:10.1146/annurev.es.11.110180.002043. DOI
Hoppe H-G. 1993. Use of fluorogenic model substrates for extracellular enzyme activity (EEA) measurement of bacteria. Lewis Publishers, Boca Raton, FL.
Eaton AD, Franson M. 2005. Standard methods for the examination of water and wastewater. American Public Health Association/American Water Works Association/Water Environment Federation, Washington, DC.
Armstrong FAJ, Stearns CR, Strickland J. 1967. The measurement of upwelling and subsequent biological process by means of the Technicon Autoanalyzer and associated equipment. Deep Sea Res Oceanographic Abstr 14:381–389. doi:10.1016/0011-7471(67)90082-4. DOI
Coleman AW. 1980. Enhanced detection of bacteria in natural environments by fluorochrome staining of DNA. Limnol Oceanogr 25:948–951. doi:10.4319/lo.1980.25.5.0948. DOI
Jochem F. 2001. Morphology and DNA content of bacterioplankton in the northern Gulf of Mexico: analysis by epifluorescence microscopy and flow cytometry. Aquat Microb Ecol 25:179–194. doi:10.3354/ame025179. DOI
Marie D, Partensky F, Jacquet S, Vaulot D. 1997. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl Environ Microbiol 63:186–193. doi:10.1128/AEM.63.1.186-193.1997. PubMed DOI PMC
Medina-Sánchez JM, Herrera G, Durán C, Villar-Argaiz M, Carrillo P. 2017. Optode use to evaluate microbial planktonic respiration in oligotrophic ecosystems as an indicator of environmental stress. Aquat Sci 79:529–541. doi:10.1007/s00027-016-0515-y. DOI
Kirchman D, K’nees E, Hodson R. 1985. Leucine incorporation and its potential as a measure of protein-synthesis by bacteria in natural aquatic system. Appl Environ Microbiol 49:599–607. doi:10.1128/AEM.49.3.599-607.1985. PubMed DOI PMC
Simon M, Azam F. 1989. Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51:201–213. doi:10.3354/meps051201. DOI
Fukuda R, Ogawa H, Nagata T, Koike I. 1998. Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64:3352–3358. doi:10.1128/AEM.64.9.3352-3358.1998. PubMed DOI PMC
Nercessian O, Noyes E, Kalyuzhnaya MG, Lidstrom ME, Chistoserdova L. 2005. Bacterial populations active in metabolism of C-1 compounds in the sediment of Lake Washington, a freshwater lake. Appl Environ Microbiol 71:6885–6899. doi:10.1128/AEM.71.11.6885-6899.2005. PubMed DOI PMC
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO. 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1. doi:10.1093/nar/gks808. PubMed DOI PMC
Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12. doi:10.14806/ej.17.1.200. DOI
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. doi:10.1038/nmeth.3869. PubMed DOI PMC
Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. doi:10.1093/nar/gkm864. PubMed DOI PMC
Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, Hugenholtz P. 2018. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36:996–1004. doi:10.1038/nbt.4229. PubMed DOI
Koblížek M. 2015. Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiol Rev 39:854–870. doi:10.1093/femsre/fuv032. PubMed DOI
Yutin N, Suzuki MT, Béjà O. 2005. Novel primers reveal wider diversity among marine aerobic anoxygenic phototrophs. Appl Environ Microbiol 71:8958–8962. doi:10.1128/AEM.71.12.8958-8962.2005. PubMed DOI PMC
Fish J, Chai B, Wang Q, Sun Y, Brown CT, Tiedje J, Cole J. 2013. FunGene: the functional gene pipeline and repository. Front Microbiol 4:291. doi:10.3389/fmicb.2013.00291. PubMed DOI PMC
Andrei A-Ş, Salcher MM, Mehrshad M, Rychtecký P, Znachor P, Ghai R. 2019. Niche-directed evolution modulates genome architecture in freshwater Planctomycetes. ISME J 13:1056–1071. doi:10.1038/s41396-018-0332-5. PubMed DOI PMC
Mehrshad M, Salcher MM, Okazaki Y, Nakano S-I, Šimek K, Andrei A-S, Ghai R. 2018. Hidden in plain sight: highly abundant and diverse planktonic freshwater Chloroflexi. Microbiome 6:176. doi:10.1186/s40168-018-0563-8. PubMed DOI PMC
Piwosz K, Shabarova T, Pernthaler J, Posch T, Šimek K, Porcal P, Salcher MM. 2020. Bacterial and eukaryotic small-subunit amplicon data do not provide a quantitative picture of microbial communities, but they are reliable in the context of ecological interpretations. mSphere 5:e00052-20. doi:10.1128/mSphere.00052-20. PubMed DOI PMC
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. doi:10.1186/s13059-014-0550-8. PubMed DOI PMC
Ter Braak CJ, Šmilauer P. 2012. Canoco reference manual and user’s guide: software for ordination, version 5.0. Microcomputer Power, Ithaca, NY.
Diversity dynamics of aerobic anoxygenic phototrophic bacteria in a freshwater lake
Photoheterotrophy by aerobic anoxygenic bacteria modulates carbon fluxes in a freshwater lake
Common Presence of Phototrophic Gemmatimonadota in Temperate Freshwater Lakes