Biogeographical and Biodiversity Patterns of Marine Planktonic Bacteria Spanning from the South China Sea across the Gulf of Bengal to the Northern Arabian Sea

Abstract

Understanding the biogeographical and biodiversity patterns of bacterial communities is essential in unraveling their responses to future environmental changes. However, the relationships between marine planktonic bacterial biodiversity and seawater chlorophyll a are largely understudied. Here, we used high-throughput sequencing to study the biodiversity patterns of marine planktonic bacteria across a broad chlorophyll a gradient spanning from the South China Sea across the Gulf of Bengal to the northern Arabian Sea. We found that the biogeographical patterns of marine planktonic bacteria complied with the scenario of homogeneous selection, with chlorophyll a concentration being the key environmental selecting variable of bacteria taxa. The relative abundance of Prochlorococcus, the SAR11 clade, the SAR116 clade, and the SAR86 clade significantly decreased in habitats with high chlorophyll a concentrations (>0.5 μg/L). Free-living bacteria (FLB) and particle-associated bacteria (PAB) displayed contrasting alpha diversity and chlorophyll a relationships with a positive linear correlation for FLB but a negative correlation for PAB. We further found that PAB had a narrower niche breadth of chlorophyll a than did FLB, with far fewer bacterial taxa being favored at higher chlorophyll a concentrations. Higher chlorophyll a concentrations were linked to the enhanced stochastic drift and reduced beta diversity of PAB but to the weakened homogeneous selection, enhanced dispersal limitation, and increased beta diversity of FLB. Taken together, our findings might broaden our knowledge about the biogeography of marine planktonic bacteria and advance the understanding of bacterial roles in predicting ecosystem functioning under future environmental changes that are derived from eutrophication. IMPORTANCE One of the long-standing interests of biogeography is to explore diversity patterns and uncover their underlying mechanisms. Despite intensive studies on the responses of eukaryotic communities to chlorophyll a concentrations, we know little about how changes in seawater chlorophyll a concentrations affect free-living bacteria (FLB) and particle-associated bacteria (PAB) diversity patterns in natural systems. Our biogeography study demonstrated that marine FLB and PAB displayed contrasting diversity and chlorophyll a relationships and exhibited completely different assembly mechanisms. Our findings broaden our knowledge about the biogeographical and biodiversity patterns of marine planktonic bacteria in nature systems and suggest that PAB and FLB should be considered independently in predicting marine ecosystem functioning under future frequent eutrophication.

Keywords: biogeography; diversity pattern; marine planktonic bacteria; niche breadth; species sorting.

FIG 1

The locations of the sampling sites. The sites were colored by the annual chlorophyll a before the sampling time. The data were obtained from the NASA MODIS ocean color website (https://oceancolor.gsfc.nasa.gov/).

FIG 2

The alpha diversity of the OTU richness, Faith’s phylogenetic diversity (Faith’s PD), and Shannon index of the total bacteria (TB) (A, D, and G), particle-associated bacteria (PAB) (B, E, and H), and free-living bacteria (FLB) (C, F, and I) along the gradient of the measured chlorophyll a concentrations.

FIG 3

Threshold indicator taxa analysis of the change points of both particle-associated bacteria (PAB) (A) and free-living bacteria (FLB) (B) in response to the measured chlorophyll a gradient as well as their overall niche breadth of the measured chlorophyll a (C). Red and dark blue symbols and areas show the magnitude of the summed z scores of increasing (z+) or decreasing (z−) taxa with an increasing chlorophyll a gradient. The peaks in the values indicate points along the measured chlorophyll a gradient that produce large amounts of change in the community structure. The number of OTUs that significantly increased (z+) or decreased (z−) with an increasing chlorophyll a value is also shown in the figure. Significant (P < 0.05) differences among groups are indicated by different alphabetic letters above the bars.

FIG 4

The dominant taxon (phyla, subphyla, clades, or lineages) distributions of both particle-associated bacteria (PAB)(A) and free-living bacteria (FLB) (B), according to different measured chlorophyll a groups. LCC, low chlorophyll a concentrations (chlorophyll a < 0.2 μg/L); MCC, medium chlorophyll a concentrations (0.2 μg/L < chlorophyll a < 0.5 μg/L); HCC, high chlorophyll a concentrations (chlorophyll a > 0.5 μg/L). In each clade or lineage, the number of OTUs that significantly increased (z+) or decreased (z−) with an increasing chlorophyll a concentration is also shown in the figure.

FIG 5

The nonmetric multidimensional scaling (NMDS) plots derived from the Bray-Curtis dissimilarities of particle-associated bacteria (PAB) and free-living bacteria (FLB) across different sampling sites (A) or in different measured chlorophyll a groups (B) as well as the beta diversity of both PAB (C) and FLB (D) in different chlorophyll a groups. LCC, low chlorophyll a concentrations (chlorophyll a < 0.2 μg/L); MCC, medium chlorophyll a concentrations (0.2 μg/L < chlorophyll a < 0.5 μg/L); and HCC, high chlorophyll a concentrations (chlorophyll a > 0.5 μg/L). Significant (P < 0.05) differences among groups are indicated by different alphabetic letters above the bars.

FIG 6

The relative importance of community assembly processes of particle-associated bacteria (PAB) (A–C) and free-living bacteria (FLB) (D–F) within groups of different chlorophyll a concentrations. The community assembly processes include homogeneous and heterogeneous selection, dispersal limitations, homogenizing dispersal, and the drift and other fractions. LCC, low chlorophyll a concentrations (chlorophyll a < 0.2 μg/L); MCC, medium chlorophyll a concentrations (0.2 μg/L < chlorophyll a < 0.5 μg/L); and HCC, high chlorophyll a concentrations (chlorophyll a > 0.5 μg/L).