Competition for ammonium between plant roots and nitrifying and heterotrophic bacteria and the effects of protozoan grazing

Verhagen, Frank J. M.; Laanbroek, Hendrikus J.; Woldendorp, J. W.

doi:10.1007/bf00010477

Cited by 98 publications

(61 citation statements)

References 32 publications

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“…These bacteria obtain energy for growth from the oxidation of ammonia and acquire the majority of their carbon through the fixation of CO 2 via the Calvin cycle. Since these microorganisms must compete with plants and other microorganisms that assimilate ammonia for biosynthesis (47,48), it is likely that they have developed adaptive strategies to cope with periods of ammonia starvation. Both Nitrosomonas cryotolerans and Nitrosomonas europaea have been shown to be particularly resilient to energy source deprivation.…”

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Transcription of All amoC Copies Is Associated with Recovery of Nitrosomonas europaea from Ammonia Starvation

2007

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The chemolithotrophic ammonia-oxidizing bacterium Nitrosomonas europaea is known to be highly resistant to starvation conditions. The transcriptional response of N. europaea to ammonia addition following short-and long-term starvation was examined by primer extension and S1 nuclease protection analyses of genes encoding enzymes for ammonia oxidation (amoCAB operons) and CO 2 fixation (cbbLS), a third, lone copy of amoC (amoC 3 ), and two representative housekeeping genes (glyA and rpsJ). Primer extension analysis of RNA isolated from growing, starved, and recovering cells revealed two differentially regulated promoters upstream of the two amoCAB operons. The distal 70 type amoCAB promoter was constitutively active in the presence of ammonia, but the proximal promoter was only active when cells were recovering from ammonia starvation. The lone, divergent copy of amoC (amoC 3 ) was expressed only during recovery. Both the proximal amoC 1,2 promoter and the amoC 3 promoter are similar to gram-negative E promoters, thus implicating E in the regulation of the recovery response. Although modeling of subunit interactions suggested that a nonconservative proline substitution in AmoC 3 may modify the activity of the holoenzyme, characterization of a ⌬amoC 3 strain showed no significant difference in starvation recovery under conditions evaluated. In contrast to the amo transcripts, a delayed appearance of transcripts for a gene required for CO 2 fixation (cbbL) suggested that its transcription is retarded until sufficient energy is available. Overall, these data revealed a programmed exit from starvation likely involving regulation by E and the coordinated regulation of catabolic and anabolic genes.Ammonia-oxidizing bacteria fulfill an important biological role because they carry out the first reaction in the oxidative pathway of the nitrogen cycle. These bacteria obtain energy for growth from the oxidation of ammonia and acquire the majority of their carbon through the fixation of CO 2 via the Calvin cycle. Since these microorganisms must compete with plants and other microorganisms that assimilate ammonia for biosynthesis (47, 48), it is likely that they have developed adaptive strategies to cope with periods of ammonia starvation. Both Nitrosomonas cryotolerans and Nitrosomonas europaea have been shown to be particularly resilient to energy source deprivation. Following 10 weeks of starvation, N. cryotolerans retained 85% of initial viability, showed no apparent degradation of DNA, protein, or RNA, and maintained an active electron transport system (21). Studies of N. europaea demonstrated persistence of the AmoB protein and immediate oxidation of added ammonia following 1 year of starvation for ammonia (38,51). This remarkable resistance to starvation likely reflects unique physiological facets of these highly specialized microorganisms. In this study, we examined transcription of genes for key energy-generating (ammonia oxidation) and energyconsuming (CO 2 fixation) reactions during recovery of N. europaea from ammo...

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Transcription of All amoC Copies Is Associated with Recovery of Nitrosomonas europaea from Ammonia Starvation

2007

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“…AOB often live in close proximity to nitrite-oxidizing bacteria and together they convert the most reduced form of nitrogen (NH 4 ϩ ) to the most oxidized (NO 3 Ϫ ) (40). In nature, AOB often face longer periods of NH 4 ϩ starvation and limitation due to low nitrogen input, low mineralization rates, or competition with other AOB (8), heterotrophic bacteria (48, 49), or plants (5,6,50). In order to respond rapidly when NH 4 ϩ becomes available, AOB must maintain their ability to oxidize NH 4 ϩ during these periods.…”

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Influence of Starvation on Potential Ammonia-Oxidizing Activity and amoA mRNA Levels of Nitrosospira briensis

Bollmann

Schmidt

Saunders

et al. 2005

Appl Environ Microbiol

143

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The effect of short-term ammonia starvation on Nitrosospira briensis was investigated. The ammonia-oxidizing activity was determined in a concentrated cell suspension with a NO x biosensor. The apparent halfsaturation constant [K m(app) ] value of the NH 3 oxidation of N. briensis was 3 M NH 3 for cultures grown both in continuous and batch cultures as determined by a NO x biosensor. Cells grown on the wall of the vessel had a lower K m(app) value of 1.8 M NH 3 . Nonstarving cultures of N. briensis showed potential ammonia-oxidizing activities of between 200 to 250 M N h ؊1 , and this activity decreased only slowly during starvation up to 10 days. Within 10 min after the addition of fresh NH 4 ؉ , 100% activity was regained. Parallel with activity measurements, amoA mRNA and 16S rRNA were investigated. No changes were observed in the 16S rRNA, but a relative decrease of amoA mRNA was observed during the starvation period. During resuscitation, an increase in amoA mRNA expression was detected simultaneously. The patterns of the soluble protein fraction of a 2-week-starved culture of N. briensis showed only small differences in comparison to a nonstarved control. From these results we conclude that N. briensis cells remain in a state allowing fast recovery of ammoniaoxidizing activity after addition of NH 4 ؉ to a starved culture. Maintaining cells in this kind of active state could be the survival strategy of ammonia-oxidizing bacteria in nature under fluctuating NH 4 ؉ availability.Chemolithoautotrophic ammonia-oxidizing bacteria (AOB) generate their energy by oxidizing ammonia (NH 3 ) to nitrite (NO 2 Ϫ ) and fix carbon via the Calvin cycle (3, 53). The oxidation of NH 3 to NO 2 Ϫ is a two-step process, where NH 3 is first oxidized to hydroxylamine (NH 2 OH) catalyzed by ammonia monooxygenase. The NH 2 OH is further oxidized to NO 2 Ϫ catalyzed by the hydroxylamine oxidoreductase, which is the energy-generating step of the ammonia oxidation (3, 53). AOB often live in close proximity to nitrite-oxidizing bacteria and together they convert the most reduced form of nitrogen (NH 4 ϩ ) to the most oxidized (NO 3 Ϫ ) (40). In nature, AOB often face longer periods of NH 4 ϩ starvation and limitation due to low nitrogen input, low mineralization rates, or competition with other AOB (8), heterotrophic bacteria (48, 49), or plants (5,6,50). In order to respond rapidly when NH 4 ϩ becomes available, AOB must maintain their ability to oxidize NH 4 ϩ during these periods. With the exception of a few marine strains within the genus Nitrosococcus (of the ␥-subclass of the Proteobacteria), all known AOB belong to a distinct clade within the ␤-subclass of the Proteobacteria (13), which comprises 11 clusters (37). By using 16S rRNA gene and more recently amoA gene sequencing, directly from environmental samples, the distribution of the members of the different clusters of AOB has been correlated to the characteristics of the environments (29, 37). The starvation behavior of several AOB belonging to different phylogenetic groups ...

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“…On the other hand, aquatic plants assimilate and incorporate inorganic nitrogen into organic matter and a significant part of this nitrogen can be supplied from the sediment (Short and McRoy 1984;Caffrey and Kemp 1992;Pedersen and Borum 1992). The plant therefore competes with nitrifying and denitrifying bacteria for nitrogen, and recent results have shown that roots of angiosperms may be better competitors than nitrifiers for NH,+ in the sediment (Verhagen et al 1995). Whether the presence of rooted aquatic plants stimulates or reduces bacterial nitrification-denitrification activity will depend on the balance between these opposing effects of root 0, release and root N uptake.…”

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Nitrification and denitrification in the rhizosphere of the aquatic macrophyte Lobelia dortmanna L.

1997

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Nitrogen and 0, transformations were studied in sediments covered by Lobelia dortmanna L.; a combination of 15N isotope pairing and microsensor (0,, NO,-, and NH,+) techniques were used. Transformation rates and microprofiles were compared with data obtained in bare sediments. The two types of sediment were incubated in doublecompartment chambers connected to a continuous flow-through system.The presence of L. dortmanna profoundly influenced both the nitrification-clenitrification activity and porewater profiles of 0,, NO,-, and NH,+ within the sediment. The rate of coupled nitrification-denitrification was greater than sixfold higher in L. dormanna-vegetated sediment than in bare sediment throughout the light-dark cycle. Illumination of the Lobelia sediment reduced denitrification activity by -30%. In contrast, this process was unaffected by light-dark shifts in the bare sediment. Oxygen microprofiles showed that 0, was released from the L. dortmanna roots to the surrounding sediment both during illumination and in darkness. This release of 0, expanded the oxic sediment volume and stimulated nitrification, shown by the high concentrations of NO,-(-30 yM) that accumulated within the rhizosphere. Both '"NZ isotope and microsensor data showed that the root-associated nitrification site was surrounded by two sites of denitrification above and below, and this led to a more efficient coupling between nitrification and denitrification in the Lobelia sediment than in the bare sediment.

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Competition for ammonium between plant roots and nitrifying and heterotrophic bacteria and the effects of protozoan grazing

Cited by 98 publications

References 32 publications

Transcription of All amoC Copies Is Associated with Recovery of Nitrosomonas europaea from Ammonia Starvation

Transcription of All amoC Copies Is Associated with Recovery of Nitrosomonas europaea from Ammonia Starvation

Influence of Starvation on Potential Ammonia-Oxidizing Activity and amoA mRNA Levels of Nitrosospira briensis

Nitrification and denitrification in the rhizosphere of the aquatic macrophyte Lobelia dortmanna L.

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