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Chapter 6 : Physiology and Genomics of Ammonia-Oxidizing

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Abstract:

This chapter is divided into two major sections: a brief comparative description of the physiology of ammonia-oxidizing (AOA) in relation to the better-characterized ammonia-oxidizing bacteria (AOB); and a discussion of features that have been gleaned from the genome sequence and its relevance to environmental genomic studies. An understanding of copper homeostasis is fundamental to the understanding of ecological success of the AOA. The genome sequence points to two types of enzyme systems that may be involved in copper handling or response to oxidative stress: genes encoding multicopper oxidases and DsbA-type proteins. Early metagenomics studies and the genome sequence of the sponge symbiont provided an indication of a capacity for ammonia oxidation. Genomic and metagenomic studies have now shed initial light on the gene inventory of mesophilic AOA. These studies indicate not only that a tremendous diversity of may thrive by ammonia oxidation but also that a distinct biochemistry of ammonia oxidation serves energy conservation in these organisms. Broad temperature range, as well as oligotrophy among AOA, shows that apparently unfavorable thermodynamics of ammonia oxidation and the requirement of reverse electron transport for biosynthetic needs do not pose significant limitations on the competitiveness of archaeal nitrifiers for scarce energy resources such as ammonia.

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6

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Figures

Image of FIGURE 1
FIGURE 1

Phylogenetic tree of based on 16S rRNA sequences (more than 800 bp, ≈800 sequences). Clades containing recognized candidate species and enrichment cultures are shown in black. Clades containing environmental clones potentially linking to ammonia oxidation are shown in gray. SAGMCG I, South African Gold Mine Crenarchaeotic Group I; HWCG, Hot Water Crenarchaeotic Group. Group I.1a is known as marine group I , and Group I.1b is known as soil

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 2
FIGURE 2

Cryo-electron tomographic section of a cell. CM, cytoplasmic membrane; SL, S layer; Rib, ribosome; Nuc, nucleoid; EDM, electron-dense matter. (Picture courtesy of Ziheng Yu and Grant Jensen.)

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 3
FIGURE 3

Stoichiometry and kinetics of ammonia oxidation by (A) Trace of oxygen uptake by aliquots of early-stationary phase cells (cell density, ~5.0 × 10 cells ml, 1 mM nitrite) obtained by microrespirometry. Ammonium added to resting cells was oxidized without significant lag time with a ratio of 1 mol of ammonium to 1.5 mol of O. (B) Michaelis-Menten kinetics calculated from oxygen uptake rates (second part) in panel A.

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 4
FIGURE 4

Diagram of the circular chromosome. Rings, from outside to the center: 1, genes of forward strand (color by COG categories); 2, genes on reverse strand (color by COG categories); 3, RNA genes (tRNAs orange, rRNAs red, other RNAs black); 4, copper-containing protein genes (red); 5, genes involved in transcription and regulation (green); 6, genes annotated as transporters (blue); 7, putative ammonia-monooxygenase genes (silver); 8, G+C content; 9, GC skew.

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 5
FIGURE 5

Archaeal genome size and G+C content. Csym, ; Nmar,

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 6
FIGURE 6

Synteny plot comparing and genomes. The comparison was done in the protein level with the program Promer ( ). The DNA sequences were translated in all six reading frames and compared.

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 7
FIGURE 7

Amino acid utilization of the largest gene in and surface proteins. The data on surface proteins ( = 38) are adapted from .

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 8
FIGURE 8

Relative contribution in COGs among representative and AOB.

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 9
FIGURE 9

Organization of the gene clusters in archaeal and bacterial nitrifiers. Putative gene names and the gene locus numbers are shown within each ORF (gray arrows). The identification and size of proteins encoded in the locus are (216 amino acids), hypothetical protein (120 amino acids), (189 amino acids), and (190 amino acids).

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 10
FIGURE 10

Proposed archaeal ammonia-oxidation pathway. NXOR, putative nitroxyl oxidoreductase; CuHAO, copper hydroxylamine oxidoreductase. The dashed line indicates the pathway having hydroxylamine as intermediate. Octagons containing Q and QH represent the oxidized and reduced quinone pool, respectively. Each complex is numbered: complex I, NADH:ubiquinone oxidoreductase; complex III, cytochrome -ubiquinone oxidoreductase; complex IV, terminal oxidase; complex V, ATP synthase. Plastocyanin-like electron carriers are shown as hexagons containing pcy.

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 11
FIGURE 11

Alignment of copper-containing nitrite reductase/multicopper oxidase gene sequences (Nmar_1259 and 1667, annotated as ) with Global Ocean Sampling data sets and cultured microorganisms. Shading of amino acids: identical (white on black) and similar (black on gray) sequences.

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 12
FIGURE 12

Proposed autotrophic 3-hydroxypropionate/4-hydroxybutyrate pathway in Enzymes catalyzing each reaction are numbered. Annotated genes are coded as a locus tag in parentheses.

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 13
FIGURE 13

Glycolysis and gluconeogenesis pathway of and the distribution of genes of enzymes involved in the process among some and

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 14
FIGURE 14

The first evidence of ectoine and hydroxyectoine biosynthesis in the (A) Comparison of ectoine synthesis operon clusters with putative gene names. Microorganisms, except for , are of marine origin. Nmar_1346, , -2,4-diaminobutyric acid acetyltransferase; Nmar_1345, , diaminobutyrate-2-oxoglutarate aminotransferase; Nmar_1344, , ectoine synthase; Nmar_1343, , ectoine hydroxylase; , aspartate kinase. (B) Phylogenetic relationship of gene. The evolutionary history was inferred using the neighbor-joining method. The evolutionary distances were computed using the JTT matrix-based method and are in the units of inferred amino acid substitutions per site. The scale bar shows 0.1 substitutions per site. The bootstrap values greater than 70% (1,000 replicates) are shown next to each node. There were a total of 130 positions in the final data set, and all positions containing gaps and missing data were eliminated from the data set.

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 15
FIGURE 15

Hierarchical clustering of and other archaeal genomes based on enzyme (A) and COG (B) clustering methods for the type of protein/functional families. The figures were prepared by using the genome-clustering tool in the integrated microbial genomes system ( ). The placement in the tree reflects the distance between genomes, whereby the computed distance is based on the similarity of the functional characterization of genomes in terms of a specific protein/functional family. The enzyme-based clustering supports an affiliation of and with the , whereas the COG-based clustering indicates that these two genera are of independent origin and possibly represent a novel kingdom (Thaumarchaeota).

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 16
FIGURE 16

Recruitment of GOS and HOT sequences to the (A) All available data sets. (B) Pelagic data sets (sampling sites are deeper than 200 m). (C) Coastal data sets (sampling sites are shallower than 200 m). (D) Surface data sets (samples are collected shallower than 200 m). (E) Deep water data sets (samples are collected deeper than 200 m). (F) Pelagic and coastal data sets against genome. Arrows indicate the position of 16S/23S rRNA genes.

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Image of FIGURE 17
FIGURE 17

Relative abundance of the number of reads in metagenomic libraries recruited to the genome. The number of reads in each metagenomic libraries is normalized by the obtained total number of reads ( = 5,773) in all libraries tested (reads are obtained from 58 libraries among 92 marine and freshwater libraries examined).

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
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Tables

Generic image for table
TABLE 1

Comparison of kinetic characteristics of ammonia oxidation by , AOB, enrichment cultures, and in situ kinetics of nitrification in natural samples, as well as ammonia assimilation by phytoplankton and heterotrophic microorganisms

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
Generic image for table
TABLE 2

Genome features of and related and AOB

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6
Generic image for table
TABLE 3

Features of genomes and crenarchaeal gene fragments

Citation: Urakawa H, Martens-Habbena W, Stahl D. 2011. Physiology and Genomics of Ammonia-Oxidizing , p 117-155. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch6

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