Time series assessment of Thaumarchaeota ecotypes in Monterey Bay reveals the importance of water column position in predicting distribution–environment relationships

Abstract

Nitrification plays a key role in marine ecosystems where Thaumarchaeota are thought to be responsible for most of the ammonia oxidation in the water column. Over a 2‐yr, near‐monthly time series at two sites in Monterey Bay we observed repeatable seasonal and depth‐based patterns of Thaumarchaeota ecotype abundance that highlighted a clear delineation between populations in shallow euphotic (< 50 m) vs. deeper mesopelagic (60–500 m) depths. Euphotic depths show greater seasonality and influence from light, while mesopelagic waters have trends based on water mass and other covarying features with depth. Three major ecotypes were recovered: a Nitrosopumilus‐like (NP) group, a Nitrosopelagicus‐like ecotype containing “shallow” water column A (WCA) members, and an ecotype affiliated with the “deep” water column B (WCB) Thaumarchaeota. These ecotypes show a strong depth distribution, with WCB dominant at ≥ 200 m depth and WCA most abundant in surface (5–100 m) waters. The NP ecotype was found throughout the water column with the highest abundance in summer, and was the only ecotype showing a correlation with measured nitrification rates. We also found three abundant taxa related to Nitrospina—the major nitrite‐oxidizing bacteria in the ocean; these showed clear connections to each of the three Thaumarchaeota ecotypes, suggesting a specific relationship between both steps of nitrification. Our results support the importance of ecotype‐based analysis of Thaumarchaeota and show that their abundance and distribution are controlled based on their water column position, with a distinct shift at 50 m between euphotic and mesopelagic depths.

Spatiotemporal Distribution of Key Pelagic Microbes in a Seasonal Oxygen-Deficient Coastal Upwelling System of the Eastern South Pacific Ocean

“…GALMSS analysis indicates that Thaumarchaeota was the microbial group with the greater percentage of predictability associated with its spatial and temporal variability (Table 1), and with all the other variables (oxygen, nitrate, ammonium and nitrate), associated with substrates and products of nitrification. In general, these results support a recent report considering the water column position (euphotic, 50 m, and deeper waters 60 -500 m) and other factors such as hydrographic explanatory variables, including oxygen, nitrite and ammonium Thaumarchaeota contribution to total microbial community (iTag-16S rRNA) variability in the Monterey Bay coastal time series (Tolar et al, 2020). However, in the case of the time series off Concepción the Thaumarchaeota depth distribution is resolved within a shallow water column depth (92 m depth).…”

“…AOA in the study area were found to be associated to the candidate order Nitrosopumilales (Stieglmeier et al, 2014), and to other ecotypes, i.e., Water Column Surface clade (WCA) with one culture Candidate Nitrosopelagicus brevis and Water Column Deep clades (WCB), as in other coastal marine time series (e.g., Beman et al, 2008;Santoro et al, 2010Santoro et al, , 2015Reji et al, 2019;Tolar et al, 2020). The ammonia-oxidizing assemblages were predominantly characterized by N. maritimus-like followed by WCA amoA reaching higher abundances during winter, whereas the deep WCB amoA ecotype showing maxima during summer at the bottom.…”

“…Indeed, WCA and N. maritimus amoA ecotypes are the main AOA in the study area in terms of the abundances of amoA genes and transcripts, and related to ammonium oxidation (Molina et al, 2010;Bristow et al, 2016;Levipan et al, 2016). In addition, both archaeal ecotypes, but mainly WCA, appear to have an important role in the ammonium oxidation in other marine ecosystems; e.g., the Gulf of California (Beman et al, 2008), Monterey Bay (Smith et al, 2014;Tolar et al, 2020), from the equatorial Pacific to the Arctic (Shiozaki et al, 2016), and the suboxic zone of the central Baltic Sea (Labrenz et al, 2010). Nonetheless, N. maritimus-like ecotypes may be less abundant at lower latitudes of the ETSP (∼12 and 18 • S; Peng et al, 2013).…”

“…Coastal marine areas hold a diverse microbial community but with the predominance of abundant taxa, such as Gammaand Alpha-proteobacteria, Bacteroidetes among other bacterial phyla, and archaea from Thaumarchaea and MGII Euryarchaea which has been reported to have a spatialtemporal dynamics, e.g., surface versus subsurface, and in response to climatic and oceanographic conditions, e.g., San Pedro Ocean Time series station (Cram et al, 2015;Parada and Fuhrman, 2017); Monterey Bay (Reji et al, 2019;Tolar et al, 2020), based on their ecological and metabolic traits (e.g., Northwest Mediterranean coast, Galand et al, 2018;Monterey Bay, Reji et al, 2019). Marine microbes from coastal zones are also subjected to anthropological pressure, such as, nutrient fertilization and other pollutants, influencing biogeochemical conditions and oxygen-deficiency (Cavicchioli et al, 2019).…”

“…However, there are still relatively few marine time series studies related to the variability of major marine archaeal lineages, besides ammonia oxidizing assemblages, especially in highly productive, oxygen-deficient and dynamic coastal upwelling areas. For example, exhaustive studies have been carried out along the California coast at San Pedro Ocean time series (SPOT) and Monterey Bay Aquarium Research Institute (MBARI) time series (e.g., Murray et al, 1999;Mincer et al, 2007;Beman et al, 2010Beman et al, , 2011Steele et al, 2011;Robidart et al, 2012;Parada and Fuhrman, 2017;Tolar et al, 2020), at the station ALOHA in Hawai (Karner et al, 2001), at Devil's Hole in Bermuda (Parsons et al, 2015), and in marine ecosystems such as Chesapeake Bay (Bouskill et al, 2011), the Mediterranean Sea (Galand et al, 2010(Galand et al, , 2018Lambert et al, 2019), and the North Sea (Wuchter et al, 2006). These studies concluded that AOA are the main responsible for ammonia oxidation in oceanic and coastal areas in general.…”