Thaumarchaeal ecotype distributions across the equatorial Pacific Ocean and their potential roles in nitrification and sinking flux attenuation

Abstract

Thaumarchaea are among the most abundant microbial groups in the ocean, but controls on their abundance and the distribution and metabolic potential of different subpopulations are poorly constrained. Here, two ecotypes of ammonia-oxidizing thaumarchaea were quantified using ammonia monooxygenase (amoA) genes across the equatorial Pacific Ocean. The shallow, or water column "A" (WCA), ecotype was the most abundant ecotype at the depths of maximum nitrification rates, and its abundance correlated with other biogeochemical indicators of remineralization such as NO 3 : Si and total Hg. Metagenomes contained thaumarchaeal genes encoding for the catalytic subunit of the urease enzyme (ureC) at all depths, suggesting that members of both WCA and the deep, water column "B" (WCB) ecotypes may contain ureC. Coupled urea hydrolysisammonia oxidation rates were similar to ammonia oxidation rates alone, suggesting that urea could be an important source of ammonia for mesopelagic ammonia oxidizers. Potential inducement of metal limitation of both ammonia oxidation and urea hydrolysis was demonstrated via additions of a strong metal chelator. The water column inventory of WCA was correlated with the depth-integrated abundance of WCB, with both likely controlled by the flux of sinking particulate organic matter, providing strong evidence of vertical connectivity between the ecotypes. Further, depth-integrated amoA gene abundance and nitrification rates were correlated with particulate organic nitrogen flux measured by contemporaneously deployed sediment traps. Together, the results refine our understanding of the controls on thaumarchaeal distributions in the ocean, and provide new insights on the relationship between material flux and microbial communities in the mesopelagic.

Depth distributions of nitrite reductase (nirK) gene variants reveal spatial dynamics of thaumarchaeal ecotype populations in coastal Monterey Bay

“…Spatial trends in the normalized abundances of thaumarchaeal rpoB , amoA and nirK suggested an increasing numerical dominance of Thaumarchaeota with depth (Fig. ), in agreement with numerous surveys in marine systems previously (e.g., Santoro et al ., ; Müller et al ., ). At both stations, abundances of the three genes were highest in the upper mesopelagic depths (80 and 100 m) as well as at 500 m. In contrast, the shallow euphotic depths (i.e., 30 m at M1 and 40 m at M2) had substantially lower abundances of the three genes (<2% of the total community).…”

“…Vertical niche partitioning between thaumarchaeal ecotypes has been evident in qPCR abundances of amoA variants (Beman et al, 2008;Santoro et al, 2010;Smith et al, 2014;Sintes et al, 2016;Smith et al, 2016;Santoro et al, 2017;Müller et al, 2018). Inferring these differential distribution patterns based on nirK abundances, however, had not been attempted so far.…”

“…Marine water column surveys have suggested the division of Thaumarchaeota into ecologically distinct phylotypes (or ecotypes), which are thought to represent vertically segregated sub-populations occupying differential niche spaces in the pelagic realm (Francis et al, 2005;Hallam et al, 2006a;Beman et al, 2008;Santoro et al, 2010;Smith et al, 2014;Smith et al, 2016;Santoro et al, 2017;Müller et al, 2018). Three primary ecotype clades have been described: (i) the Nitrosopumilus-like clade, distributed across diverse environments including marine, estuarine and terrestrial systems; (ii) the water column group A (WCA) clade, primarily found in the upper mesopelagic (<200 m); and (iii) the water column group B (WCB) clade, occupying deeper waters.…”

Free‐living chemoautotrophic and particle‐attached heterotrophic prokaryotes dominate microbial assemblages along a pelagic redox gradient

“…At least two ecotypes exist within the Thaumarchaeal nitrifying clade whose identity can be distinguished by their ammonia monooxygenase gene ( amoA ) sequence (Francis et al ., ). These two ecotypes exhibit different niche preferences and unique functional roles in the ocean (Santoro et al ., ). Further research is required to identify whether 16S rRNA phylogeny is sufficient to describe the ecophysiology of the other Archaea identified in our study and, thus, may explain why differentiation among clades between size fractions is not evident.…”

Overlooked Genetic Diversity of Ammonia Oxidizing Archaea Lineages in the Global Oceans

“…Since the first phylogenetic analysis of AOA amoA gene in the ocean (Francis et al, 2005), two groups, water column A (WCA) and water column B (WCB), were reported as the major groups of AOA in the oceanic waters, and they were proposed as two ecotypes predominating in upper (<200 m) and deep (>200 m) layers, respectively (Beman et al, 2008;Francis et al, 2005;Santoro et al, 2017). So far, there is only one culture of WCA (Nitrosopelagicus brevis CN25) reported (Santoro & Santoro & Casciotti, 2011;Santoro et al, 2015) and the WCB is still uncultivated; therefore, the physiology of these two ecotypes is still unclear (Santoro et al, 2017). In spite of this unclearness, several factors have been hypothesized as potentially causing the vertical succession of WCA and WCB, including light inhibition, differential affinities and utilization of nitrogen sources, and different requirements of micronutrients (Amin et al, 2013;Luo et al, 2014;Qin et al, 2014;Santoro et al, 2017;Sintes et al, 2013Sintes et al, , 2016Smith et al, 2016).…”