Elevated Contribution of Low Nucleic Acid Prokaryotes and Viral Lysis to the Prokaryotic Community Along the Nutrient Gradient From an Estuary to Open Ocean Transect.

Chen Hu,Xiaowei Chen,Liuqian Yu,Dapeng Xu,Nianzhi Jiao

doi:10.3389/fmicb.2020.612053

Abstract

Prokaryotes represent the largest living biomass reservoir in aquatic environments and play a crucial role in the global ocean. However, the factors that shape the abundance and potential growth rate of the ecologically distinct prokaryotic subgroups [i.e., high nucleic acid (HNA) and low nucleic acid (LNA) cells] along varying trophic conditions in the ocean remain poorly understood. This study conducted a series of modified dilution experiments to investigate how the abundance and potential growth rate of HNA and LNA prokaryotes and their regulating factors (i.e., protozoan grazing and viral lysis) change along a cross-shore nutrient gradient in the northern South China Sea. The results showed that the abundance of both HNA and LNA cells was significantly positively correlated with the abundance of heterotrophic nanoflagellates and viruses, whereas only HNA abundance exhibited a significant positive correlation with nutrient level. With a decreasing nutrient concentration, the potential growth rate of the HNA subgroup declined significantly, while that of the LNA subgroup was significantly enhanced, leading to an elevated relative potential growth rate of the LNA to HNA subgroup under decreasing nutrient levels. Furthermore, our data revealed different regulatory roles of protozoan grazing and viral lysis on the HNA and LNA subgroups, with HNA suffering higher mortality pressure from grazing than from lysis in contrast to LNA, which experienced equivalent pressures. As the nutrient levels declined, the relative contribution of lysis to the mortality of the HNA subgroup increased significantly, in contrast to the insignificant change in that of the LNA subgroup. Our results indicated the elevated role of LNA cells in the prokaryotic community and the enhanced viral lysis pressure on the total prokaryotes under oligotrophic conditions. This implies a weakened efficiency of carbon cycling within the microbial loop and enhanced viral lysis to shunt more carbon and energy flow in the future ocean, in which oligotrophication will be strengthened due to global warming.

Highlights

Representing the largest living biomass reservoir (Suttle, 2007) and critical components of the microbial loop (Azam et al, 1983) in aquatic environments, prokaryotes play a crucial role in biogeochemical cycling in the global ocean
The spatial distribution of dissolved inorganic nitrogen (DIN) along the transect largely mirrored that of the physical variables, with higher and vertically more mixed concentrations at the station affected by the nutrient-rich river plume (i.e., A has the highest surface DIN, with mean ± standard deviation of 4.15 ± 0.06 μmol L−1), whereas distinctly lower surface (0.11–0.35 μmol L−1) but higher subsurface concentrations (0.55–3.96 μmol L−1) were observed at the other offshore stations that were minimally affected by the plume (Figure 2C)
The different responses of the abundance of the two subgroups to environmental factors were further reflected by the fact that high nucleic acid (HNA) abundance was significantly correlated with both silicate concentration and temperature, while low nucleic acid (LNA) abundance was not related to any abiotic factor

Summary

Introduction

Representing the largest living biomass reservoir (Suttle, 2007) and critical components of the microbial loop (Azam et al, 1983) in aquatic environments, prokaryotes play a crucial role in biogeochemical cycling in the global ocean. The HNA cells were proposed to be the more dynamic and actively growing fraction of the prokaryotic community (Lebaron et al, 2001; Servais et al, 2003), while the LNA cells were considered to be the potentially dormant or dead cells (Jellett et al, 1996; Gasol et al, 1999) Such a view was later challenged when the LNA cells were found to exhibit substantial heterotrophic activity, comparable to that of the HNA cells (Zubkov et al, 2001; Longnecker et al, 2005; Scharek and Latasa, 2007; Huete-Stauffer and Morán, 2012). This hypothesis and the underlying roles of the potentially different regulating factors of the HNA and LNA subgroups, as of have not been investigated

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Conclusion