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Chapter 4 : Genomics of Ammonica-Oxidizing Bacteria and Insights into Their Evolution

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Abstract:

This chapter talks about ammonium-oxidizing bacteria (AOB), addresses the inventory involved in nitrification, attempts metabolic reconstruction of N transformation processes, and provides insights into their evolution. The AOB oxidizes ammonia aerobically as their sole source of energy and reductant belong taxonomically to two monophyletic groups in different proteobacterial classes. amoA-encoding archaea (AEA) is capable of being classified as obligate, ammonia-co-oxidizing mixotrophs, or chemoorganotrophs with nonfunctional amo genes in their genomes. While the anaerobic oxidation of methane by NC10 is coupled to denitrification, it is not yet clear whether the oxidation of ammonia is coupled to nitrite reduction. Ammonification, the production of ammonium from other nitrogen compounds, likely existed within early bacteria and archaea as a consequence of simple fermentations; however, these internal cycles did not likely increase net NH /NH availability. The core hydroxylamine ubiquinone redox module (HURM) genes are encoded by a conserved gene cluster, hao-orf2-cycAB, in all AOB. Complete sequences of the genes encoding the HURM proteins had been published from several AOB prior to obtain genome sequences and the protein structures of HAO and c554 have since been resolved.

Citation: Klotz M, Stein L. 2011. Genomics of Ammonica-Oxidizing Bacteria and Insights into Their Evolution, p 57-94. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch4

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Bacteria and Archaea
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Dissimilatory Nitrate Reduction to Ammonia
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Gene Expression and Regulation
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Image of FIGURE 1
FIGURE 1

Processes in the microbial nitrogen cycle. Oxidation states of each intermediate are indicated ( ); the pathway for archaeal ammonia oxidation is putative ( ). 1, Dinitrogen fixation; 2, aerobic dissimilatory ammonia oxidation to nitrite by bacteria; 3, aerobic dissimilatory ammonia oxidation to nitrite by archaea; 4, aerobic dissimilatory nitrite oxidation to nitrate by bacteria; 5, assimilatory or dissimilatory nitrate reduction to nitrite by microbes; 6, respiratory ammonification as the second step of dissimilatory nitrate reduction of ammonia (DNRA, 5 and 6); 7, assimilatory ammonification as the second step of assimilatory nitrate reduction of ammonia (ANRA, 5 and 7); 8, denitrifying anaerobic ammonia oxidation (anammox, typified by ANAOB); 9, classic (anaerobic) denitrification by mixotrophs and heterotrophs; 10, aerobic oxidation of hydroxylamine to nitrous oxide by AOB and ANB; 11, aerobic denitrification by AOB and ANB.

Citation: Klotz M, Stein L. 2011. Genomics of Ammonica-Oxidizing Bacteria and Insights into Their Evolution, p 57-94. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch4
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Image of FIGURE 2
FIGURE 2

Organization of ammonia and methane monooxygenase-encoding and ancillary genes in the genomes of betaproteobacterial and gammaproteobacterial AOB and in gammaproteobacterial and alphaproteobacterial MOB. Representative protein accession numbers are provided. Multiple copies of coregulated genes with near-identical sequence are indicated by indexed parentheses. The gene is present only in genomes of strains ATCC 19707 and AFC-27 but absent from and (Campbell and Klotz, unpublished). The gene is conserved in all nitrosococci but not involved in nitrification.

Citation: Klotz M, Stein L. 2011. Genomics of Ammonica-Oxidizing Bacteria and Insights into Their Evolution, p 57-94. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch4
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Image of FIGURE 3
FIGURE 3

Flow of nitrogen, carbon, and electrons in the quinone-reducing branch of AOB and ANB. Q/QH indicates the quinone/quinole pool in the plasma membrane (PM) and intracellular membrane (IM). The question mark indicates that a direct quinol oxidase function of AMO/pMMO has not yet been demonstrated. The stippled arrow indicates that the electrons extracted by HAO in ANB are not relayed by HURM into the Q-pool. Instead, these nitrificationborne electrons are transferred via soluble c552 proteins for energy conservation to pertinent terminal electron acceptors including Complex IV heme-copper oxidases that reduce oxygen or NO. The figure is modified from .

Citation: Klotz M, Stein L. 2011. Genomics of Ammonica-Oxidizing Bacteria and Insights into Their Evolution, p 57-94. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch4
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Image of FIGURE 4
FIGURE 4

Residence and organization of genes encoding the OCC protein HAO (HaoA) and electron transfer cytochrome proteins, for which catalytic activity also has been demonstrated: CycA () – NO reductase; CycB () – quinone reductase. Functions for putative expression products of the conserved genes and have not yet been elucidated. Bacteria with clade I, II, and III OCC are listed in the study by . The background arrow indicates that the direction of divergence on the phylogenetic tree of OCC proteins ( ) correlates with increasing co-organization of genes that encode interacting nitrification proteins.

Citation: Klotz M, Stein L. 2011. Genomics of Ammonica-Oxidizing Bacteria and Insights into Their Evolution, p 57-94. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch4
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Image of FIGURE 5
FIGURE 5

Flow of nitrogen and electrons in the quinone-reducing and quinol-oxidizing branches of the ETC of AOB. Basic inventory encoded in all AOB are shown together with reconstructed inventory encoded in individual genera or strains of AOB for niche adaptation. Abbreviations are explained in the text.

Citation: Klotz M, Stein L. 2011. Genomics of Ammonica-Oxidizing Bacteria and Insights into Their Evolution, p 57-94. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch4
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Image of FIGURE 6
FIGURE 6

The modular concept of N-oxide transformation relevant to ammonia oxidation and nitrification. Directions of chemical and evolutionary pathways are indicated by closed and open arrows, respectively. Filled diamonds indicate the merger of modules as discussed in the text.

Citation: Klotz M, Stein L. 2011. Genomics of Ammonica-Oxidizing Bacteria and Insights into Their Evolution, p 57-94. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch4
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Tables

Generic image for table
TABLE 1

New nomenclature for ammonia-oxidizing microorganisms

Citation: Klotz M, Stein L. 2011. Genomics of Ammonica-Oxidizing Bacteria and Insights into Their Evolution, p 57-94. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch4
Generic image for table
TABLE 2

Ongoing and completed whole-genome sequencing (WGS) projects involving nitrifying bacteria

Citation: Klotz M, Stein L. 2011. Genomics of Ammonica-Oxidizing Bacteria and Insights into Their Evolution, p 57-94. In Ward B, Arp D, Klotz M (ed), Nitrification. ASM Press, Washington, DC. doi: 10.1128/9781555817145.ch4

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