Abstract
In the marine environment, the abundance of Bacteria and Archaea is either controlled bottom-up via nutrient availability or top-down via grazing. Heterotrophic nanoflagellates (HNF) are mainly responsible for prokaryotic grazing losses besides viral lysis. However, the grazing specificity of HNF on specific bacterial and archaeal taxa is under debate. Bacteria and Archaea might have different nutritive values and surface properties affecting the growth rates of HNF. In this study, we offered different bacterial and archaeal strains with different morphologic and physiologic characteristics to Cafeteria roenbergensis, one of the most abundant and ubiquitous species of HNF in the ocean. Two Nitrosopumilus maritimus-related strains isolated from the northern Adriatic Sea (Nitrosopumilus adriaticus, Nitrosopumilus piranensis), two Nitrosococcus strains, and two fast growing marine Bacteria (Pseudoalteromonas sp. and Marinobacter sp.) were fed to Cafeteria cultures. Cafeteria roenbergensis exhibited high growth rates when feeding on Pseudoalteromonas sp., Marinobacter sp., and Nitrosopumilus adriaticus, while the addition of the other strains resulted in minimal growth. Taken together, our data suggest that the differences in growth of Cafeteria roenbergensis associated to grazing on different thaumarchaeal and bacterial strains are likely due to the subtle metabolic, cell size, and physiological differences between different bacterial and thaumarchaeal taxa. Moreover, Nitrosopumilus adriaticus experienced a similar grazing pressure by Cafeteria roenbergensis as compared to the other strains, suggesting that other HNF may also prey on Archaea which might have important consequences on the global biogeochemical cycles.
References
Azam F, Fenchel T, Field JG, Gray JS, Meyerreil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263
Jürgens K, Matz C (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Van Leeuwenhoek 81:413–434
Weitz JS, Wilhelm SW (2012) Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol Rep 4:17
Boenigk J, Arndt H (2002) Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Antonie Van Leeuwenhoek 81:465–480
Šimek K, Kojecká P, Nedoma J, Hartman P, Vrba J, Dolan JR (1999) Shifts in bacterial community composition associated with different microzooplankton size fractions in a eutrophic reservoir. Limnol Oceanogr 44:1634–1644
Pace ML (1988) Bacterial mortality and the fate of bacterial production. Hydrobiologia 159:41–49
Hahn MW, Höfle MG (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 35:113–121
Fenchel T (1982) Ecology of heterotrophic microflagellates .1. Some important forms and their functional-morphology. Mar Ecol Prog Ser 8:211–223
Pomeroy LR, Williams PJI, Azam F, Hobbie JE (2007) The microbial loop. Oceanography 20:28–33
Pernthaler J (2005) Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3:537–546
Sherr BF, Sherr EB, Fallon RD (1987) Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl Environ Microbiol 53:958–965
Herndl GJ, Reinthaler T, Teira E, van Aken H, Veth C, Pernthaler A, Pernthaler J (2005) Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol 71:2303–2309
Wuchter C, Abbas B, Coolen MJ, Herfort L, van Bleijswijk J, Timmers P, Strous M, Teira E, Herndl GJ, Middelburg JJ, Schouten S, Sinninghe Damste JS (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci U S A 103:12317–12322
Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510
DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89:5685–5689
Coutinho FH, Meirelles PM, Moreira AP, Paranhos RP, Dutilh BE, Thompson FL (2015) Niche distribution and influence of environmental parameters in marine microbial communities: a systematic review. PeerJ 3:e1008
Hatzenpichler R (2012) Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol 78:7501–7510
Teira E, Lebaron P, van Aken H, Herndl GJ (2006) Distribution and activity of bacteria and archaea in the deep water masses of the North Atlantic. Limnol Oceanogr 51:2131–2144
Ballen-Segura M, Felip M, Catalan J (2017) Some mixotrophic flagellate species selectively graze on archaea. Appl Environ Microbiol 83
Anderson R, Winter C, Jurgens K (2012) Protist grazing and viral lysis as prokaryotic mortality factors at Baltic Sea oxic-anoxic interfaces. Mar Ecol Prog Ser 467:1–14
Bayer B, Vojvoda J, Offre P, Alves RJ, Elisabeth NH, Garcia JA, Volland JM, Srivastava A, Schleper C, Herndl GJ (2016) Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation. ISME J 10:1051–1063
Lassak K, Neiner T, Ghosh A, Klingl A, Wirth R, Albers SV (2012) Molecular analysis of the crenarchaeal flagellum. Mol Microbiol 83:110–124
Sherr BF, Sherr EB, Rassoulzadegan F (1988) Rates of digestion of bacteria by marine phagotrophic protozoa: temperature dependence. Appl Environ Microbiol 54:1091–1095
Gonzalez JM, Iriberri J, Egea L, Barcina I (1990) Differential rates of digestion of bacteria by freshwater and marine phagotrophic protozoa. Appl Environ Microbiol 56:1851–1857
Matz C, Jurgens K (2005) High motility reduces grazing mortality of planktonic bacteria. Appl Environ Microbiol 71:921–929
Posch T, Simek K, Vrba J, Pernthaler S, Nedoma J, Sattler B, Sonntag B, Psenner R (1999) Predator-induced changes of bacterial size-structure and productivity studied on an experimental microbial community. Aquat Microb Ecol 18:235–246
Simek K, Grujcic V, Hahn MW, Hornak K, Jezberova J, Kasalicky V, Nedoma J, Salcher MM, Shabarova T (2018) Bacterial prey food characteristics modulate community growth response of freshwater bacterivorous flagellates. Limnol Oceanogr 63:484–502
Straile D (1997) Gross growth efficiencies of protozoan and metazoan zooplankton and their dependence on food concentration, predator-prey weight ratio, and taxonomic group. Limnol Oceanogr 42:1375–1385
Del Giorgio PA, Gasol JM, Vaque D, Mura P, Agusti S, Duarte CM (1996) Bacterioplankton community structure: protists control net production and the proportion of active bacteria in a coastal marine community. Limnol Oceanogr 41:1169–1179
Watson SW (1965) Characteristics of a marine nitrifying bacterium, Nitrosocystis oceanus sp. n. Limnol Oceanogr 10:274–289
Ward BB, O'Mullan GD (2002) Worldwide distribution of Nitrosococcus oceani, a marine ammonia-oxidizing gamma-proteobacterium, detected by PCR and sequencing of 16S rRNA and amoA genes. Appl Environ Microbiol 68:4153–4157
Grujcic V, Kasalicky V, Simek K (2015) Prey-specific growth responses of freshwater flagellate communities induced by morphologically distinct bacteria from the genus Limnohabitans. Appl Environ Microbiol 81:4993–5002
Hahn MW, Höfle MG (1999) Flagellate predation on a bacterial model community: interplay of size-selective grazing, specific bacterial cell size, and bacterial community composition. Appl Environ Microbiol 65:4863–4872
Boenigk J, Matz AC, Jurgens K, Arndt H (2001) Confusing selective feeding with differential digestion in bacterivorous nanoflagellates. J Eukaryot Microbiol 48:425–432
Hansen B, Bjornsen PK, Hansen PJ (1994) The size ratio between planktonic predators and their prey. Limnol Oceanogr 39:395–403
Šimek K, Kasalicky V, Jezbera J, Hornak K, Nedoma J, Hahn MW, Bass D, Jost S, Boenigk J (2013) Differential freshwater flagellate community response to bacterial food quality with a focus on Limnohabitans bacteria. ISME J 7:1519–1530
Sintes E, Del Giorgio PA (2014) Feedbacks between protistan single-cell activity and bacterial physiological structure reinforce the predator/prey link in microbial foodwebs. Front Microbiol 5:453
Acknowledgments
We thank B. Bayer for providing the two archaeal strains and F.W. Valois for providing the two Nitrosococcus strains.
Funding
Laboratory work was supported by the Austrian Science Fund (FWF) projects Z194-B17 and P28781-B21 and by the European Research Council under the European Community’s Seventh Framework Program (FP7/2007-2013)/ERC grant agreement No. 268595 (MEDEA project) to GJH. DDC was supported by the Marie Curie Fellowship (PIEF-GA-2011-299860) and by overseas researcher under the Postdoctoral Fellowship of Japan Society for Promotion of Science (P16085), and ES was supported by Austrian Science Fund (FWF) project P27696-B22.
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Figure S1
Changes over the course of the incubation experiment of C. roenbergensis and prokaryotic abundance in different treatments amended with: a) Pseudoalteromonas sp., b) Marinobacter sp., c) Nitrosopumilus adriaticus, d) Nitrosopumilus piranensis, e) Nitrosococcus oceani_27, f) Nitrosococcus oceani_107. The asterisks represent the time points when the CARD-FISH samples were collected. (PDF 534 kb)
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De Corte, D., Paredes, G., Yokokawa, T. et al. Differential Response of Cafeteria roenbergensis to Different Bacterial and Archaeal Prey Characteristics. Microb Ecol 78, 1–5 (2019). https://doi.org/10.1007/s00248-018-1293-y
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DOI: https://doi.org/10.1007/s00248-018-1293-y