Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers

Abstract

Nitrification is a core process in the global nitrogen cycle that is essential for the functioning of many ecosystems. The discovery of autotrophic ammonia-oxidizing archaea (AOA) within the phylum Thaumarchaeota has changed our perception of the microbiology of nitrification, in particular since their numerical dominance over ammonia-oxidizing bacteria (AOB) in many environments has been revealed. These and other data have led to a widely held assumption that all amoA-encoding members of the Thaumarchaeota (AEA) are autotrophic nitrifiers. In this study, 52 municipal and industrial wastewater treatment plants were screened for the presence of AEA and AOB. Thaumarchaeota carrying amoA were detected in high abundance only in four industrial plants. In one plant, thaumarchaeotes closely related to soil group I.1b outnumbered AOB up to 10,000-fold, and their numbers, which can only be explained by active growth in this continuous culture system, were two to three orders of magnitude higher than could be sustained by autotrophic ammonia oxidation. Consistently, 14 CO 2 fixation could only be detected in AOB but not in AEA in actively nitrifying sludge from this plant via FISH combined with microautoradiography. Furthermore, in situ transcription of archaeal amoA, and very weak in situ labeling of crenarchaeol after addition of 13 CO 2 , was independent of the addition of ammonium. These data demonstrate that some amoA-carrying group I.1b Thaumarchaeota are not obligate chemolithoautotrophs.heterotrophy | physiology | modeling | ammonia monooxygenase

Vertical segregation and phylogenetic characterization of ammonia-oxidizing Archaea in a deep oligotrophic lake

“…In some cases it has been reported that the archaeal amoA gene could be an evolutionary relict that is not functional anymore (Mussmann et al, 2011). Nonetheless, in Lake Redon the match found between the vertical abundance of nitrite and peaks in the abundance of both amoA and 16 S rRNA genes strongly suggests potential active ammonium oxidation zones related to archaea.…”

Metabolic potential of fatty acid oxidation and anaerobic respiration by abundant members of Thaumarchaeota and Thermoplasmata in deep anoxic peat

“…All six carbon fixation pathways known to date (Berg et al, 2010) were incomplete or undetectable in Fn1 (Supplementary Figure S5a). This latter feature is distinct from other sequenced thaumarchaeal and autotrophic crenarchaeal genomes (Berg et al, 2010;Beam et al, 2014;Konneke et al, 2014), further building on previous evidence which suggests a more versatile metabolism for members of the Phylum Thaumarchaeota (for example, bacterial ectosymbionts (Muller et al, 2010) and facultative ammonia oxidizers (Mussmann et al, 2011)). Fn1 is not predicted to ferment pyruvate to end products such as acetate, butyrate, ethanol, H 2 , lactate, and propionate (Supplementary Table S3).…”

Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume

“…Despite their abundance and biogeochemical importance, fundamental questions remain regarding the physiology and metabolism of MGI. Several studies of MGI have provided evidence for both autotrophic ammonia oxidation (Konneke et al, 2005;Ingalls et al, 2006) and heterotrophy (Ouverney and Fuhrman, 2000;Agogué et al, 2008;Mubmann et al, 2011;Tourna et al, 2011). Autotrophic ammonia oxidation has now been confirmed in a few cultured representatives (De La Torre et al, 2008;Tourna et al, 2011), including Nitrosopumilus maritimus (Konneke et al, 2005).…”

“…Whereas studies of cultures and surface waters indicate autotrophy, observations of a lower ratio of MGI amoA to 16S rRNA gene copies (Agogué et al, 2008) and decreasing MGI carbon fixation with depth (Varela et al, 2011) in the Atlantic suggest that deep-sea MGI are predominantly organoheterotrophic. Recent studies also show that the presence (and expression) of amoA genes does not necessarily indicate CO 2 fixation (Mubmann et al, 2011;Tourna et al, 2011). The GB metagenome contains genes homologous to N. maritimus genes encoding the 3-hydroxypropionate/ 4-hydroxybutyrate pathway for CO 2 fixation (Berg et al, 2007), including 4-hydroxybutyryl-CoA dehydratase, methylmalonyl-CoA epimerase and mutase, and acetyl-CoA carboxylase.…”

“…However, metagenomic sequencing of North Pacific waters at 4000 m depth revealed an equal ratio of MGI amoA to 16S rRNA genes (Konstantidis et al, 2009). Furthermore, it has recently been shown that expression of ammonia monoxygenase does not always signify autotrophy (Mubmann et al, 2011). In this study, we utilize deep-sea hydrothermal vent plumes in the Guaymas Basin (GB) of the Gulf of California as natural laboratories in which to study ecological and physiological responses of deep-sea MGI to ammonium inputs.…”