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

Verónica Molina,Osvaldo Ulloa,Héctor A Levipan,Cristóbal Anguita,Alexander Galán,Ivonne Montes,Lucy Belmar,Salvador Ramírez-Flandes

doi:10.3389/fmars.2020.561597

Abstract

The strong seasonal variability in physical-chemical conditions of the Eastern South Pacific Ocean creates an ideal setting to study spatiotemporal distribution of key marine microbial communities.. We herein report a nearly 4-year-long time series of the variability in amoA gene counts of ammonia oxidizing archaea (AOA) and bacteria (betaproteobacteria, bAOB) by quantitative PCR, GI.1a Thaumarchaeota and MG-II Euryarchaeota by CARD-FISH, and the picoplanktonic community by flow cytometry for this area. During spring-summer, non-photosynthetic picoplankton such as MG-II Euryarchaeota and GI.1a Thaumarchaeota peaked at the surface and deeper waters, respectively. General AOA and bAOB achieved higher abundances at the oxycline mainly in summer (up to 105-104 amoA copies mL-1). Generalized additive models for location, scale, and shape (GAMLSS) indicated that season and depth account for 19-46% of variations in the abundance of the groups studied, particularly GI.1a Thaumarchaeota and AOA. The oxygen and nitrite concentration were statistically meaningful predictors for the studied groups. GAMLSS models indicate that ammonia oxidizing assemblage’s variability is coupled with ammonia, nitrite, and nitrate variations. Our results indicate that microbial abundances fluctuation is associated with upwelling variability and oxygen-deficient water conditions that shape the substrates availability and metabolic response of marine microbes, including keystone ammonia oxidizing assemblages and their ecological interactions. Overall, our results support planktonic nitrification activity and its contribution to nitrous oxide excess production in the time series off Concepción and the ecological dynamics regarding AOA -bAOB in coastal waters.

Highlights

Two functional groups represented by ammonia- and nitrite-oxidizing microorganisms catalyze complete marine nitrification, with the rate-limited first step of this reaction performed by ammonia-oxidizing bacteria (AOB) and archaea (AOA) (Ward, 2008)
In the study area, upwelling fertilizes the surface with high-nutrient content waters fueling primary and secondary productivity (e.g., Montero et al, 2007), and develops a seasonal oxygen deficiency in the subsurface associated with Equatorial Subsurface Waters (ESSW) which was evident during our study (Ahumada and Chuecas, 1979; Sobarzo et al, 2007)
Our results indicate the physical-chemical oceanographic conditions associated with the seasonal upwelling systems modulate the distribution and dynamics of abundant marine microbial groups including key ammonia oxidizing assemblages

Summary

Introduction

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). Chemoautotrophic assemblages associated with nitrification have been reported to play a central role in the functioning of coastal microbial assemblages (e.g., network analyses, Parada and Fuhrman, 2017; Reji et al, 2020). Nitrification is a chemoautotrophic process associated with a two-steps aerobic reaction that oxidizes ammonia into nitrite followed by the conversion of nitrite into nitrate. Two functional groups represented by ammonia- and nitrite-oxidizing microorganisms catalyze complete marine nitrification, with the rate-limited first step of this reaction performed by ammonia-oxidizing bacteria (AOB) and archaea (AOA) (Ward, 2008). Nitrospira bacteria able to catalyze one-step ammonia oxidation to nitrate (Comammox) represents the only known exception to this rule (Daims et al, 2015; van Kessel et al, 2015). The biogeochemical impact of Nitrospira-like Comammox bacteria on the marine nitrogen cycle is still unclear, since these microorganisms appear to be absent in marine ecosystems (Daims et al, 2016)

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Conclusion