Characterization of particle-associated and free-living bacterial and archaeal communities along the water columns of the South China Sea

Jiangtao Li,Lei Su,Shijie Bai,Li Zhang,Lingyuan Gu,Bingbing Wei,Jiasong Fang,Jie Wang

doi:10.5194/bg-18-113-2021

Abstract

Abstract. There is a growing recognition of the role of particle-attached (PA) and free-living (FL) microorganisms in marine carbon cycle. However, current understanding of PA and FL microbial communities is largely focused on those in the upper photic zone, and relatively fewer studies have focused on microbial communities of the deep ocean. Moreover, archaeal populations receive even less attention. In this study, we determined bacterial and archaeal community structures of both the PA and FL assemblages at different depths, from the surface to the bathypelagic zone along two water column profiles in the South China Sea. Our results suggest that environmental parameters including depth, seawater age, salinity, particulate organic carbon (POC), dissolved organic carbon (DOC), dissolved oxygen (DO) and silicate play a role in structuring these microbial communities. Generally, the PA microbial communities had relatively low abundance and diversity compared with the FL microbial communities at most depths. Further microbial community analysis revealed that PA and FL fractions generally accommodate significantly divergent microbial compositions at each depth. The PA bacterial communities mainly comprise members of Alphaproteobacteria and Gammaproteobacteria, together with some from Planctomycetes and Deltaproteobacteria, while the FL bacterial lineages are also mostly distributed within Alphaproteobacteria and Gammaproteobacteria, along with other abundant members chiefly from Actinobacteria, Cyanobacteria, Bacteroidetes, Marinimicrobia and Deltaproteobacteria. Moreover, there was an obvious shifting in the dominant PA and FL bacterial compositions along the depth profiles from the surface to the bathypelagic deep. By contrast, both PA and FL archaeal communities dominantly consisted of euryarchaeotal Marine Group II (MGII) and thaumarchaeotal Nitrosopumilales, together with variable amounts of Marine Group III (MGIII), Methanosarcinales, Marine Benthic Group A (MBG-A) and Woesearchaeota. However, the pronounced distinction of archaeal community compositions between PA and FL fractions was observed at a finer taxonomic level. A high proportion of overlap of microbial compositions between PA and FL fractions implies that most microorganisms are potentially generalists with PA and FL dual lifestyles for versatile metabolic flexibility. In addition, microbial distribution along the depth profile indicates a potential vertical connectivity between the surface-specific microbial lineages and those in the deep ocean, likely through microbial attachment to sinking particles.

Highlights

The sinking of particulate organic matter (POM) formed in the photic layer is a fundamental process that transports carbon and nutrient materials from the surface into the usually starved deep ocean, with a significant role in structuring the distributions and activities of marine microorganisms in the dark realm (Azam and Malfatti, 2007; Mestre et al, 2018; Suter et al, 2018)
Some broad key functional gene categories involved in dissolved organic matter (DOM) utilization (Poretsky et al, 2010; Rinta-Kanto et al, 2012) and specific functional gene groups linked to successive decomposition of phytoplankton blooms (Teeling et al, 2012) are significantly different, indicating the fundamental differences in survival strategies in relation to potentially available substrates
The PA fraction is relatively enriched in members of Gammaproteobacteria, Verrucomicrobia, Bacteroidetes, Firmicutes and Planctomycetes (Azam and Malfatti, 2007; Milici et al, 2016; Salazar et al, 2016; Suter et al, 2018), while the FL assemblages are often populated by members of Alphaproteobacteria (SAR11 clade or Candidatus Pelagibacter) and Deferribacteres (DeLong et al, 1993; Crespo et al, 2013; Milici et al, 2017)

Summary

Introduction

The sinking of particulate organic matter (POM) formed in the photic layer is a fundamental process that transports carbon and nutrient materials from the surface into the usually starved deep ocean, with a significant role in structuring the distributions and activities of marine microorganisms in the dark realm (Azam and Malfatti, 2007; Mestre et al, 2018; Suter et al, 2018). PA bacteria, compared to FL bacteria, are often larger in size (Alldredge et al, 1986; Zhang et al, 2007; Lauro et al, 2009) and metabolically more active (Karner and Herdl, 1992; Grossart et al, 2007). They often maintain higher levels of extracellular enzymes, adhesion proteins, and antagonistic compounds and are capable of degrading high-molecular-weight (HMW) organic compounds (Smith et al, 1992; Crump et al, 1998; Long and Azam, 2001; Mevel et al, 2008; Ganesh et al, 2014). Significantly overlapped compositions of PA and FL microbial communities were reported in a few studies (Hollibaugh et al, 2000; Ghiglione et al, 2007; OrtegaRetuerta et al, 2013; Rieck et al, 2015; Liu et al, 2018a)

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Discussion

Conclusion