Microorganisms are the majority of life in the ocean and play fundamental roles in ecological functions and biogeochemical cycles (Fuhrman, 2009). Advances in genomics have revealed vertical zonation of planktonic microbial communities, which reflects the nature of ocean stratification (Giovannoni et al., 1996; DeLong et al., 2006; Shi et al., 2011). For example, the photic zone is characterized by steep gradients of light, temperature (thermocline), salinity (halocline), and nutrients (neutricline), which dictate the species distribution and function in the upper water column; in the aphotic zone (>200 m depth), decreasing temperature, increasing hydrostatic pressure and lack of light and energy supplies determine the microbial community structure and function of the dark ocean (DeLong et al., 2006). However, other physical processes such as water mass movement and mesoscale eddies have also been reported to control the distribution of microbial populations or activity in the ocean (Galand et al., 2008, 2010; Zhang et al., 2009; Chen et al., 2016).

Planktonic archaea have been recognized to play important roles in global carbon and nitrogen cycles (Karner et al., 2001; Francis et al., 2005; Ingalls et al., 2006). They were initially divided into Marine Group I (MGI; now called Thaumarchaeota) and Marine Group II (MGII) that belong to Euryarchaeota (DeLong, 1992); the latter has generally been observed to dominate the surface ocean in archaeal composition, whereas the former becomes increasingly abundant at greater depths (Massana et al., 2000; Karner et al., 2001; Herndl et al., 2005; Lincoln et al., 2014). While tremendous progress has been made in the physiology, biochemistry, and ecological functions of Thaumarchaeota (Konneke et al., 2005; Ingalls et al., 2006; Martens-Habbena et al., 2009), our understanding of the MGII in the archaeal domain remains fragmented (Zhang C.L. et al., 2015). MGII have been classified into four groups (MGIIA, MGIIB, MGIIC, and MGIID) according to their 16S rRNA gene sequences (Martin-Cuadrado et al., 2015). However, there is no pure culture of MGII at the present. Recently, the metagenomic and transcriptomic studies of MGII have been increasing and gradually unveiling their potential ecological functions in carbon and nitrogen cycling in the ocean. This is exemplified by reports on the capability of MGII in degradation of protein and lipids (Iverson et al., 2012), synthesization of archaeal tetraether lipids (Lincoln et al., 2014), utilization of dissolved protein (Orsi et al., 2015), attachment and utilization of particulate organic matter (Orsi et al., 2016), and harvesting solar energy in the photic zone using proteorhodopsin (Iverson et al., 2012; Li et al., 2015; Orsi et al., 2015, 2016). However, the mechanisms controlling the distribution of MGII in different water columns of the ocean are poorly known.

The South China Sea (SCS) is the largest marginal sea of the northwestern Pacific, which has recently witnessed significant growth in microbial and biogeochemical studies in this oceanographic region (Liu et al., 2007; Moisander et al., 2008; Zhang et al., 2009; Hu et al., 2011; Wei et al., 2011; Jia et al., 2012; Jiao et al., 2014a; Tseng et al., 2015; Xia et al., 2015). The water column dynamics of the SCS is regulated by complex basin topography and water circulations resulting from East Asian Monsoon activities and the Pacific Kuroshio current intrusion (Xu and Oey, 2015; Zhang Z. et al., 2015). Occurrence of surface-confined phototrophic populations in deep waters has been observed in the western Pacific, Luzon Strait, and the SCS, which may be attributed to the active vertical mixing and isopycnal heaving of water associated with internal solitary waves, mesoscale eddies, and/or other physical processes (Jiao et al., 2014b; Chen et al., 2016). A recent study also observed the impact of asymmetrical internal solitary waves on temperature, nutrients, and chlorophyll a in the northern SCS (Dong et al., 2015).

Although the archaeal and bacterial community structures have been reported to be influenced by strong internal waves in the western Pacific Ocean near Luzon Strait (Jiao et al., 2014a), as well as to be affected by mesoscale cyclonic eddies in the western and the central northern SCS, the distributional patterns and niche specificity of archaea in the northeastern SCS are still unknown. The aim of this study was to unveil the relative abundance and distribution of ammonia-oxidizing archaea (AOA) and bacteria (AOB), MGII and total bacteria by targeting the archaeal and bacterial ammonia monooxygenase (amoA) genes and the 16S rRNA genes of MGII and bacteria, respectively, using qPCR. The archaeal community structure was also determined by using 454 sequencing. Overall, we examined that the archaeal community structure showed great similarity between different water depths in the northeastern SCS, which was different from the archaeal community structure presented in western and central regions of the SCS (Zhang et al., 2009). We also observed that the relative abundance of AOA was low throughout the whole water column (Figures 2, 3) compared to other regions of the SCS (Hu et al., 2011). These results collectively suggest that the predominance of MGII in archaeal composition throughout the water column of the northeastern SCS may be caused by strong vertical mixing in this region (Tian et al., 2009; Jiao et al., 2014a).

Temperature and salinity profiles were similar among the B and D stations (Supplementary Figure S1), which are typically observed in the SCS. In this study, we focused on describing the microbiological variation in Thaumarchaeota, MGII and bacteria among these stations. The abundance of Thaumarchaeota was estimated using the archaeal amoA gene based on the consensus that the ratio of archaeal amoA gene to Thaumarchaeotal 16S rRNA gene is between 1 and 2 in the open Ocean (Church et al., 2010; Hu et al., 2011; Lund et al., 2012).

The ocean is characteristically stratified, which is reflected in much stronger difference in microbial community structure vertically than horizontally (DeLong et al., 2006; Shi et al., 2011). In this study, the distribution of Thaumarchaeota, MGII, and MGIII in the northeastern SCS (B and D stations) has distinct patterns from that in other areas of the SCS (Zhang et al., 2009; Tseng et al., 2015; Xia et al., 2015). In particular, the relatively abundant MGII and MGIII distribution with depth at the B and D stations has not been reported in previous studies that mostly describe MGII being predominant in surface water whereas Thaumarchaeota or MGIII in deep water (López-García et al., 2001; Herndl et al., 2005; DeLong et al., 2006; Galand et al., 2009; Tseng et al., 2015; Zhang C.L. et al., 2015).

Jiao et al. (2014a) have reported the presence of surface picoplankton (Prochlorococcus) in deep waters in Luzon Strait in the western Pacific Ocean, who dismissed aggregation, particle packing through grazing and egestion, or winter ventilation as the mechanisms for picoplankton transport to the deep water. It is also counterintuitive that organic matter is enriched in falling particles with increasing depth because the concentration of POC has been observed to decrease with depth (Dai et al., 2009). However, it is possible that the lability of organic matter differed with changing depths at these stations, as the type of organic matter can certainly influence the physiological properties of these proposed heterotrophs. More likely, the transportation of surface water microorganisms was attributed to multiple physical processes such as internal solitary waves, meso-scale eddies and turbulent mixing in the Luzon Strait and the northeastern SCS (Jiao et al., 2014a). A recent report (Chen et al., 2016) also indicated that internal solitary waves can enhance heterotrophic bacterial growth in the northern SCS. These studies highlight the importance of physical processes in controlling the distribution of planktonic microorganisms in the SCS.

The same physical processes reported by Jiao et al. (2014a) may be responsible for the transport of shallow water MGII groups down to the deep water as well as the abundant presence of MGIII throughout the water column in the northeastern SCS, which can be inferred by the similar depth profiles and similarity matrixes of different archaeal groups. Furthermore, from the available data used in the construction of the phylogenetic tree of MGII and MGIII, sequences from the SCS are more frequently affiliated with those from the Pacific Ocean than from other regions (Figure 4), suggesting the impact of mixing between the Pacific and the SCS waters on the community structure of planktonic archaea in the latter. On the other hand, we cannot exclude the contribution of the gravitational falling of particle-attached microbes on the occurrence of MGII at greater depths.

The low abundance of autotrophic AOA (Thaumarchaeota) throughout the whole column in the northeastern SCS is in contrast to the peak abundance of AOA occurring at 50–200 m depths, which is 5- to 10-fold higher than surface AOA observed in other regions of the SCS (Hu et al., 2011). Furthermore, the low abundance of AOA (Thaumarchaeota) compared to MGII and the scarce abundance of AOB in the northeastern SCS may be possibly due to the overall oligotrophic environment that is particularly depleted in ammonium. Hu et al. (20110) also showed the scarce AOB in SCS, in which bacterial amoA gene was only detected in seven out of 26 samples (Hu et al., 2011). In our study, only one out of 60 samples contained detectable bacterial amoA genes. AOB are commonly found in soils, freshwater, estuaries, hot springs, and marine environments (Francis et al., 2005). They appear to be more abundant than AOA in coastal settings where ammonium was relatively higher than in the oligotrophic ocean (Fan et al., 2015). AOA on the other hand are more adapted to oligotrophy in the ocean because they possess much higher affinity for ammonia than AOB (Martens-Habbena et al., 2009). It has been reported that the concentration of ammonia concentration in the area near our study sites ranged from 0.08 to 0.38 μM, which is lower than other regions of the SCS (Ling, 2011). The threshold of ammonia concentration for the growth of AOA is as low as 10 nM while the minimum ammonia concentration for the growth of AOB is greater than 1 μM observed under culture conditions (Martens-Habbena et al., 2009). Thus, the lack of ammonia probably was the main reason why AOB were almost absent in our study area. On the other hand, the low abundance of AOA throughout the whole water column in the northeastern SCS may not be due to the low abundance of ammonia alone; vertical mixing could be another reason, which could homogenize low AOA surface water with relatively more AOA abundant deeper water, a hypothesis that can be tested in future studies.

It is intriguing to observe the significant correlation (R² = 0.76, Figure 6) between the abundance of MGII 16S rRNA gene copies and the abundance of bacterial 16S rRNA gene copies in the northeastern SCS. Significant correlation between MGII and total bacteria has also been observed in western and northern central SCS water column (Zhang et al., 2009) and our work in the western Pacific also supports this observation (unpublished data). Thus it is likely this correlation holds true in other regions of the global ocean. At the moment, however, we can only speculate the possible mechanisms underlying this correlation. One possibility is that the occurrence of MGII and bacteria is controlled by a common variable, for example the affinity to particles. This may be supported by the observation of Orsi et al. (2015), which showed that both MGII and heterotrophic bacterial groups prefer to attach to particles in the ocean waters. Unfortunately our study only used 0.2 μm filters for sample collection, which included possibly both free-living and particle attached bacteria and MGII. Future research is needed to test this hypothesis.

In summary, our results showed that the archaeal distributional patterns in the northeastern SCS water column were distinct from other marine regions. The most abundant archaeal MGII subgroups were MGIIA (OTU 23, 26, 27 in Figure 4) and MGIIB (other MGII OTUs in Figure 4), with the former clade being mainly present at shallow waters (<100 m) while the later clade being widely present in both shallow and deep waters. In general, the heterotrophic archaea represented by MGII were much more abundant than the autotrophic archaea Thaumarchaeota throughout the whole water column in the northeastern SCS. The exact mechanisms controlling the particular archaeal distribution patterns and community structure remain unclear because of lacking direct physical and chemical measurements as well as RNA analysis. Future studies will need to couple microbiological sampling with measurements of physical and chemical properties in time series in the SCS, which should shed light on or strengthen our understanding of how heterotrophic and autotrophic archaea respond to the changing marine environment.

CZ and HL developed the idea and designed the study. HL, CY, and SC processed and analyzed the data. HL and CZ wrote the manuscript. ZZ and JT contributed to the discussion on physical processes in the SCS. ZC contributed to the data analysis.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.