

FOLLOWUS
1.State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, China
2.State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China
3.The Philips Institute of Oral and Craniofacial Molecular Biology, Virginia Commonwealth University, Richmond, VA 23298-0566, United States of America
Limei SHI,lmshi@niglas.ac.cn
Min ZHANG,mzhang@niglas.ac.cn
Received:22 October 2021,
Accepted:08 February 2022,
Online First:02 April 2022,
Published:2022-09
Scan QR Code
Limei SHI, Yuanfeng CAI, Xiaoli SHI, et al. Community structure of aerobic anoxygenic phototrophic bacteria in algae- and macrophyte-dominated areas in Taihu Lake, China[J]. Journal of Oceanology and Limnology, 2022, 40(5): 1855-1867.
Limei SHI, Yuanfeng CAI, Xiaoli SHI, et al. Community structure of aerobic anoxygenic phototrophic bacteria in algae- and macrophyte-dominated areas in Taihu Lake, China[J]. Journal of Oceanology and Limnology, 2022, 40(5): 1855-1867. DOI: 10.1007/s00343-022-1348-2.
Aerobic anoxygenic phototrophic bacteria (AAPB) represent a major group of bacterioplankton assemblages in many water systems and some are assumed to be closely associated with phytoplankton. However
studies on relationships between AAPB and cyanobacterial blooms are in scarcity. The dynamics of the abundance and diversity of AAPB was compared based on
pufM
gene in Meiliang Bay (featured by cyanobacterial blooms) and East Bay (featured by macrophyte) of Taihu Lake
a shallow subtropical lake in the East China plain. AAPB abundance was not significantly different between the two sites
and they were positively correlated with dissolved organic carbon (DOC) concentration. The ratios of AAPB to total bacteria varied from 3.4% to 11.5% and peaked in winter in both sites. No significant differences of AAPB community compositions were detected between the two sites
but there was a separation between warm seasons (June
August
and October) and cold seasons (December
February
and April). Rhizobiales and
Limnohabitans
-like
pufM
sequences were significantly contributors for the difference between two seasons
and specially enriched in cold seasons. Chlorophyll
a
(Chl
a
) and DOC were the most significant variables influencing the AAPB community structure. Furthermore
Porphyrobacter
and Rhodospirillales-like
pufM
sequences were positively correlated with Chl
a
indicating potential influence of cyanobacterial blooms on these AAPB taxa. These results suggested that diverse AAPB ecotypes coexisted in Taihu Lake
and their ecological role in carbon cycling in the lake may not be ignored.
Achenbach L A, Carey J, Madigan M T. 2001. Photosynthetic and phylogenetic primers for detection of anoxygenic phototrophs in natural environments. Applied and Environmental Microbiology , 67 (7): 2922–2926.
Allgaier M, Uphoff H, Felske A et al. 2003. Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. Applied and Environmental Microbiology , 69 (9): 5051–5059.
Asai R, Horiguchi Y, Yoshida A et al. 2001. Detection of phycobilin pigments and their seasonal change in Lake Kasumigaura using a sensitive in situ fluorometric sensor. Analytical Letters , 34 (14): 2521–2533.
Béjà O, Suzuki M T, Heidelberg J F et al. 2002. Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature , 415 (6872): 630–633.
Berg K A, Lyra C, Sivonen K et al. 2009. High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms. The ISME Journal , 3 (3): 314–325.
Boeuf D, Cottrell M T, Kirchman D L et al. 2013. Summer community structure of aerobic anoxygenic phototrophic bacteria in the western Arctic Ocean. FEMS Microbiology Ecology , 85 (3): 417–432.
Brient L, Lengronne M, Bertrand E et al. 2008. A phycocyanin probe as a tool for monitoring cyanobacteria in freshwater bodies. Journal of Environmental Monitoring , 10 (2): 248–255.
Cai H Y, Jiang H L, Krumholz L R et al. 2014. Bacterial community composition of size-fractioned aggregates within the phycosphere of cyanobacterial blooms in a eutrophic freshwater lake. PLoS One , 9 (8): e102879.
Caliz J, Casamayor E O. 2014. Environmental controls and composition of anoxygenic photoheterotrophs in ultraoligotrophic high-altitude lakes (central Pyrenees). Environmental Microbiology Reports , 6 (2): 145–151.
Cepáková Z, Hrouzek P, Žišková E et al. 2016. High turnover rates of aerobic anoxygenic phototrophs in European freshwater lakes. Environmental Microbiology , 18 (12): 5063–5071.
Chen Y W, Qin B Q, Teubner K et al. 2003. Long-term dynamics of phytoplankton assemblages: Microcystis -domination in Lake Taihu, a large shallow lake in China. Journal of Plankton Research , 25 (4): 445–453.
Chen Y, Zhang Y, Jiao N Z. 2011. Responses of aerobic anoxygenic phototrophic bacteria to algal blooms in the East China Sea. Hydrobiologia , 661 (1): 435–443.
Cole J R, Chai B, Marsh T L et al. 2003. The ribosomal database project (RDP-Ⅱ): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Research , 31 (1): 442–443.
Čuperová Z, Holzer E, Salka I et al. 2013. Temporal changes and altitudinal distribution of aerobic anoxygenic phototrophs in mountain lakes. Appliedand Environmental Microbiology , 79 (20): 6439–6446.
Du H L, Jiao N Z, Hu Y H et al. 2006. Real-time PCR for quantification of aerobic anoxygenic phototrophic bacteria based on pufM gene in marine environment. Journal of Experimental Marine Biology and Ecology , 329 (1): 113–121.
Fauteux L, Cottrell M T, Kirchman D L et al. 2015. Patterns in abundance, cell size and pigment content of aerobic anoxygenic phototrophic bacteria along environmental gradients in northern lakes. PLoS One , 10 (4): e0124035.
Ferrera I, Borrego C M, Salazar G et al. 2014. Marked seasonality of aerobic anoxygenic phototrophic bacteria in the coastal NW Mediterranean Sea as revealed by cell abundance, pigment concentration and pyrosequencing of pufM gene. Environmental Microbiology , 16 (9): 2953–2965.
Ferrera I, Sánchez O, Kolářová E et al. 2017a. Light enhances the growth rates of natural populations of aerobic anoxygenic phototrophic bacteria. The ISME Journal , 11 (10): 2391–2393.
Ferrera I, Sarmento H, Priscu J C et al. 2017b. Diversity and distribution of freshwater aerobic anoxygenic phototrophic bacteria across a wide latitudinal gradient. Frontiers in Microbiology , 8 : 175.
Fleischman D, Kramer D. 1998. Photosynthetic rhizobia. Biochimica et Biophysica Acta (BBA) — Bioenergetics , 1364 (1): 17–36.
Giraud E, Fleischman D. 2004. Nitrogen-fixing symbiosis between photosynthetic bacteria and legumes. Photosynthesis Research , 82 (2): 115–130.
Goecke F, Thiel V, Wiese J et al. 2013. Algae as an important environment for bacteria-phylogenetic relationships among new bacterial species isolated from algae. Phycologia , 52 (1): 14–24.
Graham E D, Heidelberg J F, Tully B J. 2018. Potential for primary productivity in a globally-distributed bacterial phototroph. The ISME Journal , 12 (7): 1861–1866
Green D H, Llewellyn L E, Negri A P et al. 2004. Phylogenetic and functional diversity of the cultivable bacterial community associated with the paralytic shellfish poisoning dinoflagellate Gymnodinium catenatum . FEMS Microbiology Ecology , 47 (3): 345–357.
Hu Y H, Du H L, Jiao N Z et al. 2006. Abundant presence of the γ-like proteobacterial pufM gene in oxic seawater. FEMS Microbiology Letters , 263 (2): 200–206.
Imhoff J F, Rahn T, Künzel S et al. 2018. Photosynthesis is widely distributed among Proteobacteria as demonstrated by the phylogeny of pufLM reaction center proteins. Frontiers in Microbiology , 8 : 2679.
Jeanthon C, Boeuf D, Dahan O et al. 2011. Diversity of cultivated and metabolically active aerobic anoxygenic phototrophic bacteria along an oligotrophic gradient in the Mediterranean Sea. Biogeosciences , 8 (7): 1955–1970.
Jia T X, Zhang X Q, Dong R C. 2019. Long-term spatial and temporal monitoring of cyanobacteria blooms using MODIS on Google earth engine: a case study in Taihu Lake. Remote Sensing , 11 (19): 2269.
Jiang H C, Deng S C, Huang Q Y et al. 2010. Response of aerobic anoxygenic phototrophic bacterial diversity to environment conditions in saline lakes and Daotang River on the Tibetan Plateau, NW China. Geomicrobiology Journal , 27 (5): 400–408.
Jiang H C, Dong H L, Yu B S et al. 2009. Abundance and diversity of aerobic anoxygenic phototrophic bacteria in saline lakes on the Tibetan Plateau. FEMS Microbiology Ecology , 67 (2): 268–278.
Jiao N Z, Herndl G J, Hansell D A et al. 2010. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nature Reviews Microbiology , 8 (8): 593–599.
Jiao N Z, Zhang Y, Zeng Y H et al. 2007. Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean. Environmental Microbiology , 9 (12): 3091–3099.
Kasalický V, Zeng Y H, Piwosz K et al. 2018. Aerobic anoxygenic photosynthesis is commonly present within the genus Limnohabitans . Applied and Environmental Microbiology , 84 (1): e02116–17.
Kobližek M, Falkowski P G, Kolber Z S. 2006. Diversity and distribution of photosynthetic bacteria in the Black Sea. Deep Sea Research Part Ⅱ: Topical Studies in Oceanography , 53 (17–19): 1934–1944.
Koblížek M, Mašín M, Ras J et al. 2007. Rapid growth rates of aerobic anoxygenic phototrophs in the ocean. Environmental Microbiology , 9 (10): 2401–2406.
Koblížek M. 2015. Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiology Reviews , 39 (6): 854–870.
Kolářová E, Medová H, Piwosz K et al. 2019. Seasonal dynamics of aerobic anoxygenic phototrophs in freshwater lake Vlkov. Folia Microbiologica , 64 (5): 705–710.
Kolber Z S, Plumley F G, Lang A S et al. 2001. Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science , 292 (5526): 2492–2495.
Lehours A C, Cottrell M T, Dahan O et al. 2010. Summer distribution and diversity of aerobic anoxygenic phototrophic bacteria in the Mediterranean Sea in relation to environmental variables. FEMS Microbiology Ecology , 74 (2): 397–409.
Letunic I, Bork P. 2007. Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics , 23 (1): 127–128.
Li Q, Song A, Peng W J et al. 2017. Contribution of aerobic anoxygenic phototrophic bacteria to total organic carbon pool in aquatic system of subtropical karst catchments, Southwest China: evidence from hydrochemical and microbiological study. FEMS Microbiology Ecology , 93 (6): fix065.
Ma J R, Qin B Q, Paerl H W et al. 2016. The persistence of cyanobacterial ( Microcystis spp. ) blooms throughout winter in Lake Taihu, China. Limnology and Oceanography , 61 (2): 711–722.
Mašín M, Čuperová Z, Hojerová E et al. 2012. Distribution of aerobic anoxygenic phototrophic bacteria in glacial lakes of northern Europe. Aquatic Microbial Ecology , 66 (1): 77–86.
Masin M, Nedoma J, Pechar L et al. 2008. Distribution of aerobic anoxygenic phototrophs in temperate freshwater systems. Environmental Microbiology , 10 (8): 1988–1996.
Nadkarni M A, Martin F E, Jacques N A et al. 2002. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology , 148 (1): 257–266.
Oksanen J, Blanchet F G, Kindt R et al. 2013. Vegan: Community Ecology Package. R version 2. https://cran.r-project.org/web/packages/vegan/index.html https://cran.r-project.org/web/packages/vegan/index.html .
Paerl H W, Paul V J. 2012. Climate change: links to global expansion of harmful cyanobacteria. Water Research , 46 (5): 1349–1363.
Piwosz K, Vrdoljak A, Frenken T et al. 2020. Light and primary production shape bacterial activity and community composition of aerobic anoxygenic phototrophic bacteria in a microcosm experiment. mSphere , 5 (4): e00354–20.
Qin B Q, Xu P Z, Wu Q L et al. 2007. Environmental issues of Lake Taihu, China. Hydrobiologia , 581 (1): 3–14.
Ritchie A E, Johnson Z I. 2012. Abundance and genetic diversity of aerobic anoxygenic phototrophic bacteria of coastal regions of the Pacific Ocean. Applied and Environmental Microbiology , 78 (8): 2858–2866.
Robinson M D, McCarthy D J, Smyth G K. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics , 26 (1): 139–140.
Ruiz-González C, Garcia-Chaves M C, Ferrera I et al. 2020. Taxonomic differences shape the responses of freshwater aerobic anoxygenic phototrophic bacterial communities to light and predation. Molecular Ecology , 29 (7): 1267–1283.
Salka I, Čuperova Z, Mašín M et al. 2011. Rhodoferax -related pufM gene cluster dominates the aerobic anoxygenic phototrophic communities in German freshwater lakes. Environmental Microbiology , 13 (11): 2865–2875.
Sato-Takabe Y, Hamasaki K, Suzuki S. 2019. High temperature accelerates growth of aerobic anoxygenic phototrophic bacteria in seawater. Microbiologyopen , 8 (5): e00710.
Sato-Takabe Y, Hirose S, Hori T et al. 2020. Abundance and spatial distribution of aerobic anoxygenic phototrophic bacteria in Tama River, Japan. Water , 12 (1): 150.
Schloss P D, Westcott S L, Ryabin T et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology , 75 (23): 7537–7541.
Shi L M, Cai Y F, Chen Z T et al. 2010. Diversity and abundance of aerobic anoxygenic phototrophic bacteria in two cyanobacterial bloom-forming lakes in China. Annales de Limnologie — International Journal of Limnology , 46 (4): 233–239.
Shi L M, Cai Y F, Li P F et al. 2009a. Molecular identification of the colony-associated cultivable bacteria of the cyanobacterium Microcystis aeruginosa and their effects on algal growth. Journal of Freshwater Ecology , 24 (2): 211–218.
Shi L M, Cai Y F, Yang H L et al. 2009b. Phylogenetic diversity and specificity of bacteria associated with Microcystis aeruginosa and other cyanobacteria. Journal of Environmental Sciences , 21 (11): 1581–1590.
Tian Y Y, Wu X Q, Zhou Q C et al. 2018. Distribution of aerobic anoxygenic phototrophs in freshwater plateau lakes. Polish Journal of Environmental Studies , 27 (2): 871–879.
Tillett D, Neilan B A. 2000. Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. Journal of Phycology , 36 (1): 251–258.
Waidner L A, Kirchman D L. 2005. Aerobic anoxygenic photosynthesis genes and operons in uncultured bacteria in the Delaware River. Environmental Microbiology , 7 (12): 1896–1908.
Waidner L A, Kirchman D L. 2008. Diversity and distribution of ecotypes of the aerobic anoxygenic phototrophy gene pufM in the Delaware estuary. Applied and Environmental Microbiology , 74 (13): 4012–4021.
Xu H, Paerl H W, Zhu G W et al. 2017. Long-term nutrient trends and harmful cyanobacterial bloom potential in hypertrophic Lake Taihu, China. Hydrobiologia , 787 (1): 229–242.
Yurkov V V, Beatty J T. 1998. Aerobic anoxygenic phototrophic bacteria. Microbiology and Molecular Biology Reviews , 62 (3): 695–724.
Zeng Y H, Chen X H, Jiao N Z. 2007. Genetic diversity assessment of anoxygenic photosynthetic bacteria by distance-based grouping analysis of pufM sequences. Letters in Applied Microbiology , 45 (6): 639–645.
Zeng Y H, Kasalicky V, Simek K et al. 2012. Genome sequences of two freshwater Betaproteobacterial isolates, Limnohabitans species strains Rim28 and Rim47, indicate their capabilities as both photoautotrophs and ammonia oxidizers. Journal of Bacteriology , 194 (22): 6302–6303.
Zhang H H, Wang Y, Huang T L et al. 2020. Mixed-culture aerobic anoxygenic photosynthetic bacterial consortia reduce nitrate: core species dynamics, co-interactions and assessment in raw water of reservoirs. Bioresource Technology , 315 : 123817.
Zhang Y C, Ma R H, Liang Q C et al. 2019. Secondary impacts of eutrophication control activities in shallow lakes: lessons from aquatic macrophyte dynamics in Lake Taihu from 2000 to 2015. Freshwater Science , 38 (4): 802–817.
Zhang Y L, Liu X H, Qin B Q et al. 2016. Aquatic vegetation in response to increased eutrophication and degraded light climate in eastern Lake Taihu: implications for lake ecological restoration. Scientific Reports , 6 : 23867.
Zhang Y, Jiao N Z. 2007. Dynamics of aerobic anoxygenic phototrophic bacteria in the East China Sea. FEMS MicrobiologyEcology , 61 (3): 459–469.
Zhu C M, Zhang J Y, Wang X et al. 2021. Responses of cyanobacterial aggregate microbial communities to algal blooms. Water Research , 196 : 117014.
0
Views
0
Downloads
1
CSCD
Publicity Resources
Related Articles
Related Author
Related Institution
京公网安备11010802024621