The Distribution of Bathyarchaeota in Surface Sediments of the Pearl River Estuary Along Salinity Gradient

Abstract

Bathyarchaeota, a recently proposed archaeal phylum, is globally distributed and highly abundant in anoxic sediments. Metabolic pathways of the Bathyarchaeota members are diverse and, hence, this phylum has been proposed to play an important role in global biogeochemical cycles. Bathyarchaeota members are distributed in the estuarine environments. However, limited information is available about their detailed community structure, abundance, and functions in the Pearl River estuary (PRE). In the current study, we performed a comprehensive investigation of the archaeal community in the PRE surface sediments along a salinity gradient, with a focus on Bathyarchaeota. Bathyarchaeota was the dominant archaeal phylum, with the abundance of the bathyarchaeotal 16S rRNA gene ranging from 1.43 × 10 8 to 1.22 × 10 9 copies/g sediment dry weight (d.w.), and Bathy-8 was the dominant subgroup. Thaumarchaeota, Lokiarchaeota, and Euryarchaeota, including Thermoprofundales (MBG-D archaea), were the other major archaeal groups in the PRE. The differences of community distributions in the high-and low-salinity sediments were hence investigated. Statistical analysis revealed that besides salinity, ammonium, and total organic carbon were the most important environmental factors influencing the archaea community structure, including that of Bathyarchaeota, in the PRE. The archaeal network indicated the cooccurrence among Bathyarchaeota, Lokiarchaeota, and Euryarchaeota, while Bathy-6 presented unique correlations compared with other bathyarchaeotal subgroups. These observations indicate that Bathyarchaeota may play a role in ecosystem function through microbe-microbe interactions, revealing a possible different lifestyle for Bathy-6 in eutrophic estuarine sediments.

Community, Distribution, and Ecological Roles of Estuarine Archaea

“…AOA are suggested as major players in the nitrogen cycle in low-nutrient environments ( Erguder et al, 2009 ), such as the oligotrophic oceans ( Francis et al, 2005 ). They are also reported as the major ammonia oxidizers in some eutrophic estuaries ( Beman and Francis, 2006 ; Bernhard and Bollmann, 2010 ; Cao et al, 2011 ; Jin et al, 2011 ; Wang et al, 2014 ; Zou et al, 2019 , 2020b ) and lakes ( Wu et al, 2010 ; Hou et al, 2013 ; Zhao et al, 2013 ; Bollmann et al, 2014 ). The impact of these environmental parameters, especially the salinity and ammonium concentration, on the distribution of AOA varies with species ( Fukushima et al, 2012 ; Hatzenpichler, 2012 ; Stahl and de la Torre, 2012 ), which implies that AOA are well adapted to different environments.…”

“…Increasing numbers of archaeal groups are being recognized as vital players in estuarine biogeochemical cycles ( Figure 1 ). These include: Thaumarchaeota , which comprise ammonia oxidizing archaea (AOA), one of the key players of ammonia oxidation in estuaries ( Francis et al, 2005 ; Liu L. et al, 2011 ; Liu Z. et al, 2011 ; Zou et al, 2019 , 2020b ); Bathyarchaeota (formerly called Miscellaneous Crenarchaeotal Group, MCG), which are hypothesized to be important players in the benthic carbon cycle that, based on genomic analysis, may be able to utilize diverse organic substrates ( Meng et al, 2014 ; Lazar et al, 2015 , 2016 ; He et al, 2016 ; Zhou et al, 2018a ); Euryarchaeota , e.g., most methanogens and anaerobic methanotrophs, are responsible for methane production and oxidation in estuaries, respectively ( Oremland and Polcin, 1982 ; Serrano-Silva et al, 2014 ); and Asgard archaea, such as Thorarchaeota and Lokiarchaeota , which may participate in some biogeochemical cycles, as suggested by metagenomics ( Seitz et al, 2016 ; Liu Y. et al, 2018 ; MacLeod et al, 2019 ; Cai et al, 2020 ). Recently, Liu et al (2018b) explored the diversity and community structure of archaea in over 20 estuaries.…”

“…Salinity and other environmental parameters are important for shaping the bathyarchaeotal community in costal and estuarine regions ( Liu et al, 2014 ; Lazar et al, 2015 ; Yoshimura et al, 2018 ; Zhou et al, 2018b ; Pan et al, 2019 ; Chen Y. et al, 2020 ; Zou et al, 2020b ). The total abundance of Bathyarchaeota increases with the sediment depths in the Pearl River Estuary ( Liu et al, 2014 ), and decreases with the decreasing reductive redox conditions in the sediment in the White Oak River ( Lazar et al, 2015 ), but it remained stable in the surface sediments of the Pearl River Estuary ( Zou et al, 2020b ) and the Bay of Marennes-Oléron ( Hélène et al, 2015 ). Salinity and ammonium levels are major factors influencing the distribution of Bathyarchaeota in surface sediments of the Pearl River Estuary ( Zou et al, 2020b ).…”

“…The total abundance of Bathyarchaeota increases with the sediment depths in the Pearl River Estuary ( Liu et al, 2014 ), and decreases with the decreasing reductive redox conditions in the sediment in the White Oak River ( Lazar et al, 2015 ), but it remained stable in the surface sediments of the Pearl River Estuary ( Zou et al, 2020b ) and the Bay of Marennes-Oléron ( Hélène et al, 2015 ). Salinity and ammonium levels are major factors influencing the distribution of Bathyarchaeota in surface sediments of the Pearl River Estuary ( Zou et al, 2020b ). On the other hand, the pH and oxygen levels, rather than salinity, are contributing factors shaping community structure of Bathyarchaeota community structure in costal mangroves and lakes ( Yoshimura et al, 2018 ; Pan et al, 2019 , 2020 ).…”

Genomic and transcriptomic evidence of light-sensing, porphyrin biosynthesis, Calvin-Benson-Bassham cycle, and urea production in Bathyarchaeota

“…Based on the analysis of metagenome-assembled genomes (MAGs) and single-cell genomes (SAGs), Bathyarchaeota has been implicated to have potential abilities for CO 2 fixation with Wood-Ljungdahl pathway, acetogenesis, methane metabolism, and degradation of peptides, fatty acids, aromatic, and other organic compounds [2,3,[14][15][16][17], suggesting Bathyarchaeota may play an important role in the global carbon cycle. At least 25 subgroups have been identified in Bathyarchaeota based on the phylogenetic analyses of 16S rRNA genes [13], and many subgroups display distinct environmental preferences implicating diversification and adaptation to unique environmental conditions [6,[18][19][20][21]. Thus, the current information is too limited to comprehensively understand the metabolic capacities of Bathyarchaeota and its role in the geochemical cycle.…”