Piecewise Structural Equation Model (SEM) Disentangles the Environmental Conditions Favoring Diatom Diazotroph Associations (DDAs) in the Western Tropical North Atlantic (WTNA).

Marcus Stenegren,Joseph P Montoya,Carlo Berg,Rachel A Foster,Cory C Padilla,Patricia L Yager,Stefan-Sebastian David

doi:10.3389/fmicb.2017.00810

Abstract

Diatom diazotroph associations (DDAs) are important components in the world’s oceans, especially in the western tropical north Atlantic (WTNA), where blooms have a significant impact on carbon and nitrogen cycling. However, drivers of their abundances and distribution patterns remain unknown. Here, we examined abundance and distribution patterns for two DDA populations in relation to the Amazon River (AR) plume in the WTNA. Quantitative PCR assays, targeting two DDAs (het-1 and het-2) by their symbiont’s nifH gene, served as input in a piecewise structural equation model (SEM). Collections were made during high (spring 2010) and low (fall 2011) flow discharges of the AR. The distributions of dissolved nutrients, chlorophyll-a, and DDAs showed coherent patterns indicative of areas influenced by the AR. A symbiotic Hemiaulus hauckii-Richelia (het-2) bloom (>106 cells L-1) occurred during higher discharge of the AR and was coincident with mesohaline to oceanic (30–35) sea surface salinities (SSS), and regions devoid of dissolved inorganic nitrogen (DIN), low concentrations of both DIP (>0.1 μmol L-1) and Si (>1.0 μmol L-1). The Richelia (het-1) associated with Rhizosolenia was only present in 2010 and at lower densities (10-1.76 × 105 nifH copies L-1) than het-2 and limited to regions of oceanic SSS (>36). The het-2 symbiont detected in 2011 was associated with H. membranaceus (>103 nifH copies L-1) and were restricted to regions with mesohaline SSS (31.8–34.3), immeasurable DIN, moderate DIP (0.1–0.60 μmol L-1) and higher Si (4.19–22.1 μmol L-1). The piecewise SEM identified a profound direct negative effect of turbidity on the het-2 abundance in spring 2010, while DIP and water turbidity had a more positive influence in fall 2011, corroborating our observations of DDAs at subsurface maximas. We also found a striking difference in the influence of salinity on DDA symbionts suggesting a niche differentiation and preferences in oceanic and mesohaline salinities by het-1 and het-2, respectively. The use of the piecewise SEM to disentangle the complex and concomitant hydrography of the WTNA acting on two biogeochemically relevant populations was novel and underscores its use to predict conditions favoring abundance and distributions of microbial populations.

Highlights

Richelia intracellularis is one of the few heterocystous cyanobacteria commonly found in the oligotrophic oceans and are considered an important source of new nitrogen (N) and primary production (Mague et al, 1974; Venrick, 1974)
Following an earlier classification scheme based on sea surface salinities (SSS), three salinity categories were defined: ‘low’ SSS containing stations with SSS < 30, ‘mesohaline’ stations have SSS between 30 and 35, and stations with SSS > 35 were classified as ‘oceanic’ (Foster et al, 2007)
A summary of the stations and nutrient concentrations for the three categories is provided in Table 1, and the corresponding station locations and surface nutrient concentrations are shown in Figures 1, 2, respectively

Summary

Introduction

Richelia intracellularis is one of the few heterocystous cyanobacteria commonly found in the oligotrophic oceans and are considered an important source of new nitrogen (N) and primary production (Mague et al, 1974; Venrick, 1974). The diatom symbioses are widespread in distribution, fragile, hard to collect and recognize, and difficult to study. The diatoms and their respective diazotrophic partners are often referred to as Diatom Diazotroph Associations, or DDAs. The western tropical North Atlantic (WTNA) near the Amazon and Orinoco river plumes is an ideal location to study the presence, distribution, and activity of symbiotic diatoms, since large and expansive blooms of the DDA, Hemiaulus-Richelia, are consistently observed (Villareal, 1994; Carpenter et al, 1999; Foster et al, 2007; Subramaniam et al, 2008; Goes et al, 2014). The influence of the rivers is far-reaching and seasonal, where within the freshwater lenses, distinct phytoplankton populations and enhanced nutrient concentrations can be observed at distances greater than 1,600 km away from the river mouths (Borstad, 1982a,b; Muller-Karger et al, 1988, 1995)

Methods

Results

Discussion

Conclusion