Hydrography shapes community composition and diversity of amoA‐containing Thaumarchaeota in the coastal waters off central Chile

Abstract

Thaumarchaea are often abundant in low oxygen marine environments, and recent kinetic studies indicate a capacity for aerobic ammonia oxidation at vanishingly low oxygen levels (nM). However, molecular diversity surveys targeting this group to high sequencing coverage are limited, and how these populations are coupled to changes in dissolved oxygen remains unknown. In this study, the ammonia monooxygenase subunit A (amoA) gene was sequenced from samples collected in the Chilean coast (36.5 °S), a system prone to recurrent seasonal hypoxia and anoxia, at several depths over one year, to read depths that saturated coverage statistics. Temperature, salinity and depth displayed a stronger impact on community composition than chemical and biological variables, such as dissolved oxygen. The Nitrosopumilus water-column A clade (WCA) displayed high proportional representation in all samples (42%-100% of all amoA OTUs). The two dominant WCA OTUs displayed differences in their distributions that were inversely correlated with one another, providing the first evidence for intra-subgroup specific differences in the distributions among closely related WCA Thaumarcheota. Nitrosopumilus water-column B (WCB) representatives displayed increased proportional abundances (42%) at deeper depths during the spring and summer, were highly coupled to decreased dissolved oxygen conditions and were non-detectable during the austral winter. The depth of sequencing also enabled observation of lower abundance taxa that are typically not observed in marine environments, such as members of the genus Nitrosotalea amid austral winter surface waters. This study highlights a strong coupling between Thaumarchaeal community diversity and hydrographic variables, is the first to highlight intra-subclade depth specific shifts in community diversity amongst members of the WCA clade, and links the WCB clade to upwelling conditions associated with seasonal oxygen depletion.

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

“…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. This result was supported by previous reports in the study area based on AOA amoA survey using clone libraries (Molina et al, 2010), and iTag sequencing (Bertagnolli and Ulloa, 2017) using primers designed by Pester et al (2012). These previous studies revealed specific predominant contribution of the WCA amoA in both upwelling and non-upwelling season and of the deep WCB amoA during the upwelling period.…”

“…Recently, ammonia and nitrite oxidation has been detected in this area at nanomolar concentrations of oxygen (5-33 nM, Bristow et al, 2016). Furthermore, molecular studies indicate the presence of an abundant and rich AOA community (Molina et al, 2010;Bertagnolli and Ulloa, 2017), as well as of Nitrospina spp., as the main drivers of nitrification under oxygen-deficient conditions at bottom waters during the spring-summer time (Levipan et al, 2014). In general, the water column is characterized by higher bacterioplankton abundances in summer (Galán et al, 2012), and Nitrosopumilus maritimus predominance (an important AOA ecotype at the Sta.18) in winter months based on metagenomic data (Murillo et al, 2014).…”

Regulation of nitrous oxide production in low oxygen waters off the coast of Peru

“…Thus, our findings about regulation of N2O production at different stations probably apply to the region as a whole. Several studies indicate that water mass hydrography plays an important role in shaping microbial community diversity (Biller et al 2012, Hamdan et al 2012) and a coupling of amoA alpha diversity to physical conditions such as salinity, temperature and depth has 420 been shown in coastal waters off Chile (Bertagnolli and Ulloa 2017). While salinity, temperature and depth were prominent factors in shaping the community compositions of nitrifiers and denitrifiers ( Figure S4), for N2O production rates correlations with physical and chemical parameters were not consistent.…”

Processes and Microorganisms Involved in the Marine Nitrogen Cycle: Knowledge and Gaps

“…The structure of AOA populations follows different patterns in coastal waters. For instance, WCA organisms seem to be distributed at all depths, whereas WCB organisms are confined to low-O 2 and low-chlorophyll deeper waters in the Pacific coasts (Smith et al, 2014a;Bertagnolli and Ulloa, 2017). Additionally, AOA populations fluctuate seasonally, with abundance peaks during winter in the coastal Arctic and North Sea (Christman et al, 2011;Pitcher et al, 2011b), whereas in the Chilean coast, WCB organisms are abundant during spring and summer and non-detectable during winter (Bertagnolli and Ulloa, 2017).…”