Benthic microbial biogeography along the continental shelf shaped by substrates from the Changjiang River plume
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Abstract: Coastal zones are active reactors of continental material including that transported by rivers via a series of microbiota-mediated reactions. Nevertheless, current knowledge of the ecology and functioning of the microbiota in coastal areas affected by large riverine inputs remains insufficient on a global scale. Here, an investigation on sediment microbial composition, including taxonomy and metabolic network, as well as their relationship with major benthic reaction substrates, namely carbon, nitrogen, sulphur and phosphorus, was conducted in the continental shelf affected by the spread of the Changjiang River plume. Surface sediment samples (48 samples) were collected during March 2018, obtaining a mean Operational Taxonomic Units (OTUs) number of 3 341. Proteobacteria, Acidobacteria and Actinobacteria were abundant phyla in the studied sediments. Bray-Curtis distance analysis classified the 48 samples into 4 clusters (MG1 to MG4) at the phylum-level. MG1 and MG2 are found near the river mouth, receiving substantial land-derived particles from the Changjiang River runoff. Particle-attached microbes may be settled in these regions and influenced the observed sediment microbial diversity and biomass, e.g., increased Crenarchaeota relative abundance. The relative enrichment of these two groups in heterotrophic microbes further suggests a reliance of benthic microbiota on substrates with terrestrial origin, particularly specialized on processing sulphur-rich substrates. Regions MG3 and MG4 are located in the outer margin of the area affected by the Changjiang River plume, mainly fed by settling pelagic particles from phytoplankton. Compared to MG1 and MG2, a significant increase in the abundance of Thaumarcheota (phylum-level) and Nitrosopumilus (genus-level) was found in MG3, suggesting nitrogen-related transformations as the key reactions to sustain microbial metabolism in this region. Coupled with the identified variations in the taxonomic composition, significant differences in the keystone taxa between MG1/MG2 and MG3/MG4 were identified via OTU co-occurrence analyses. A higher abundance of Actinobacteria, Thaumarchaeota and Acidobacteria in MG3 and MG4 reinforced the identified spatial variability in benthic metabolism and highlighted the significance of substrate inputs on the sediment microbial structure and biogeography.
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Key words:
- benthic microbiota /
- biogeography /
- benthic substrate /
- Changjiang River plume /
- East China Sea /
- Yellow Sea
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Figure 1. Spatial distributions of temperature (a) and salinity (b) in surface waters (1 m below sea surface) in the continental shelf affected by the Changjiang River plume during March 2018 as measured with CTD vertical profiles. Dots represent CTD measurement sites. Spatial distribution of the 48 sediment samples collected in the continental shelf affected by the Changjiang River plume in March 2018 (c). The Changjiang River outflow (CJ), Taiwan Warm Current (TWC) and the Yellow Sea Coastal Current (YSCC) are schematically represented based on Kim et al. (2018).
Figure 2. UPGMA phylogenetic tree based on Bray-Curtis distance combined with phylum-level species distribution (a); the mean abundance of genus and OTUs in MG1, MG2, MG3 and MG4 groups (b and c).
Figure 3. Network of co-occurring OTUs in MG1 (a), MG2 (b), MG3 (c) and MG4 (d), based on correlation analysis. The selection standards for strong and significant correlation are Spearman’s ρ>0.6 and p<0.01, respectively. The size of each node is proportional to the relative abundance of each OTU in the network; the color and thickness of each connection between two nodes (edge) are proportional to the value of Spearman’s correlation coefficients. The OTUs assigned to the same phylum were marked with the same color.
Figure 4. Unweighted unifrac PCoA plots visualizing community dissimilarities and variations of environmental factors. OC represents organic carbon; TN, total nitrogen; S, sulfur; IP, inorganic phosphorus. The color code denotes the target environmental variable level.
Figure 5. Relationships of overall community structure and environmental factors obtained through RDA analysis, including contents (according to mass fraction) of organic carbon (OC), total nitrogen (TN), sulfur (S), inorganic phosphorus (IP), and proportions of clay and sand in the continental shelf samples.
Table 1. Distribution of the top 20 most dominant OTUs, the closest uncultured bacteria 16S rRNA gene fragment and the closest cultured bacteria to these dominant OTUs
MG1 MG2 MG3 MG4 Closest uncultured bacteria
(accession numbers)Identity Closest cultured bacteria
(accession numbers)Identity OTU_2 2.21%±0.99% 5.92%±1.64% 6.92%±1.38% 2.56%±0.66% uncultured gamma proteobacterium (KU173695.1) 100% Woeseia oceani strain XK5
(NR_147719.1)96% OTU_33 1.06%±0.51% 4.00%±1.78% 1.00%±0.77% 1.43%±0.48% uncultured bacterium clone (KM356694.1) 100% Thioprofundum hispidum strain gps61 (NR_112620.1) 96% OTU_1 0.91%±0.90% 0.74%±0.36% 5.69%±2.51% 1.81%±1.33% uncultured marine archaeon (KJ504342.1) 100% Nitrosopumilus cobalaminigenes strain HCA1 (NR_159206.1) 99% OTU_3 0.52%±0.34% 0.79%±0.41% 0.95%±0.05% 2.55%±0.92% uncultured bacterium (MG949250.1) 100% Desulfatiglans parachlorophenolica strain DS (NR_126176.1) 90% OTU_13 0.30%±0.20% 0.93%±0.35% 1.28%±0.67% 1.64%±0.60% uncultured bacterium (MG002285.1) 100% Sandaracinus amylolyticus strain NOSO 4 (NR_118001.1) 89% OTU_21 0.43%±0.29% 1.60%±0.47% 0.32%±0.27% 1.29%±0.43% uncultured bacterium (KX097260.1) 100% Desulfobulbus propionicus strain DSM 2032 (NR_074930.1) 93% OTU_19 1.93%±1.20% 1.31%±0.73% 0.05%±0.04% 0.83%±0.41% uncultured Chloroflexi bacterium (GU061267.1) 100% Thermomarinilinea lacunifontana strain SW7 (NR_132293.1) 90% OTU_50 0.30%±0.22% 0.64%±0.40% 3.63%±1.50% 0.96%±0.70% uncultured marine group I crenarchaeote (JN590160.1) 100% Nitrosopumilus ureiphilus strain PS0 (NR_159208.1) 97% OTU_6 4.59%±3.39% 0.36%±0.47% 0.01%±0.01% 0.22%±0.30% uncultured archaeon (KX952634.1) 100% Thermogladius calderae strain 1633 (NR_148751.1) 85% OTU_27 0.61%±0.42% 1.32%±0.24% 1.18%±0.96% 0.50%±0.32% uncultured bacterium (JN621386.1) 99% Thiohalomonas nitratireducens strain HRHd 3sp (NR_043974.1) 93% OTU_5 0.21%±0.19% 1.06%±0.72% 0.08%±0.08% 0.72%±0.29% uncultured bacterium (KM203552.1) 100% Pelobacter venetianus strain Gra PEG 1 (NR_044779.1) 93% OTU_137 0.19%±0.1% 0.40%±0.20% 1.68%±0.73% 0.82%±0.46% uncultured bacterium (EU491352.1) 99% Thioprofundum lithotrophicum strain 106 (NR_112829.1) 94% OTU_4 0.28%±0.19% 1.04%±0.42% 0.66%±0.50% 0.53%±0.41% uncultured gamma proteobacterium (KR086607.1) 100% Thiohalobacter thiocyanaticus strain HRh1 (NR_116699.1) 93% OTU_29 0.29%±0.09% 0.77%±0.37% 0.15%±0.06% 0.82%±0.30% uncultured bacterium (KP292396.1) 100% Desulfonema magnum str. Montpellier strain 4be13(NR_025990.1) 93% OTU_15 0.21%±0.20% 0.48%±0.28% 0.10%±0.17% 1.05%±0.70% uncultured bacterium (HM598581.1) 100% Thermomarinilinea lacunifontana strain SW7 (NR_132293.1) 89% OTU_18 0.01%±0.01% 0.00%±0.00% 0.43%±0.40% 1.38%±0.47% no data ND Vibrio splendidus strain CH-105 (MH713000.1) 100% OTU_57 0.27%±0.12% 0.42%±0.12% 0.89%±0.22% 0.80%±0.33% uncultured bacterium (KX957641.1) 100% Desulfosarcina alkanivorans strain PL12 (NR_157797.1) 93% OTU_59 0.22%±0.13% 0.90%±0.29% 0.16%±0.19% 0.47%±0.23% uncultured bacterium (KR825168.1) 100% Desulfobulbus propionicus strain DSM 2032 (NR_074930.1) 91% OTU_25 0.44%±0.65% 0.35%±0.08% 0.92%±0.53% 0.58%±0.19% uncultured bacterium (EU734975.1) 100% Thermodesulfovibrio aggregans strain TGE-P1 (NR_040795.1) 85% OTU_9 0.18%±0.10% 0.74%±0.25% 0.33%±0.25% 0.49%±0.14% uncultured bacterium (KC631592.1) 100% Pseudohaliea rubra strain CM41_15a (NR_044426.1) 96% 
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Table 2. The alpha diversity of the obtained four microbial groups in the sediments of the continental shelf affected by the Changjiang River plume
Richness Chao1 Shannon_2 Simpson Dominance Equitability MG1 3 337±386 3 338.49±386.00 9.38±0.50 0.007 7±0.005 0 0.990±0.005 0.80±0.04 MG2 3 463±495 3 464.57±495.00 9.20±0.40 0.009 1±0.003 0 0.990±0.003 0.78±0.03 MG3 3 391±516 3 392.54±516.00 9.38±0.30 0.006 8±0.005 0 0.990±0.005 0.80±0.03 MG4 2 789±397 2 791.24±397.00 8.55±0.30 0.014 0±0.004 0 0.980±0.004 0.75±0.02
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Table 3. Average sediment organic carbon (OC), total nitrogen (TN), sulfur (S) and inorganic phosphorus (IP) contents together with sediment particle sizes (MPS) in the four microbial groups identified through Bray-Curtis distance
OC content/% TN content/% S content/% IP content/(μmol·g−1) MPS/µm Clay content/% Silt proportion/% Sand proportion/% MG1 0.5±0.1 0.1±0.0 0.38±0.02 17.8±3.1 9.1±2.7 30.4±4.5 64.0±3.6 5.6±4.3 MG2 0.5±0.2 0.1±0.0 0.28±0.04 18.5±4.4 12.8±8.4 27±5.9 63.3±6 9.7±10.6 MG3 0.1±0.0 0.0±0.0 0.14±0.00 14.9±3.3 239.0±43.4 4.8±2.3 9.1±4.9 86.1±7.1 MG4 0.3±0.1 0.1±0.0 0.22±0.04 16.4±6.0 76.8±54.4 18.7±4.0 30.0±8.4 51.3±11.7
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