Exploring the Microdiversity Within Marine Bacterial Taxa: Toward an Integrated Biogeography in the Southern Ocean

Abstract

Most of the microbial biogeographic patterns in the oceans have been depicted at the whole community level, leaving out finer taxonomic resolution (i.e., microdiversity) that is crucial to conduct intra-population phylogeographic study, as commonly done for macroorganisms. Here, we present a new approach to unravel the bacterial phylogeographic patterns combining community-wide survey by 16S rRNA gene metabarcoding and intra-species resolution through the oligotyping method, allowing robust estimations of genetic and phylogeographic indices, and migration parameters. As a proof-of-concept, we focused on the bacterial genus Spirochaeta across three distant biogeographic provinces of the Southern Ocean; maritime Antarctica, sub-Antarctic Islands, and Patagonia. Each targeted Spirochaeta operational taxonomic units were characterized by a substantial intrapopulation microdiversity, and significant genetic differentiation and phylogeographic structure among the three provinces. Gene flow estimations among Spirochaeta populations support the role of the Antarctic Polar Front as a biogeographic barrier to bacterial dispersal between Antarctic and sub-Antarctic provinces. Conversely, the Antarctic Circumpolar Current appears as the main driver of gene flow, connecting sub-Antarctic Islands with Patagonia and maritime Antarctica. Additionally, historical processes (drift and dispersal limitation) govern up to 86% of the spatial turnover among Spirochaeta populations. Overall, our approach bridges the gap between microbial and macrobial ecology by revealing strong congruency with macroorganisms distribution patterns at the populational level, shaped by the same oceanographic structures and ecological processes.

Keywords: Antarctic Circumpolar Current; Antarctic Polar Front; Microbial Conveyor Belt; Minimum Entropy Decomposition; Southern Ocean; Spirochaeta; microdiversity; phylogeography.

FIGURE 1

Sampling localities across the Southern Ocean, encompassing Possession Bay and Puerto Deseado in Atlantic Patagonia (PAT1 and PAT2, respectively), King George Island in Maritime Antarctica (KGI), and Port-aux-Français in Kerguelen Islands (KER). The Antarctic Polar Front (APF) and the Southern Antarctic Circumpolar Front (SACCF) are represented by the limit between the white and the blue areas, and by the dashed line, respectively.

FIGURE 2

Non-metric multidimensional scaling scatter diagram of the Spirochaeta OTUs composition in gut tissue samples across the localities. Presence/absence matrix converted in Bray–Curtis distances (A) and Unweighted Unifrac distance (B). Colors are assigned to the locality.

FIGURE 3

Clustering of Spirochaeta OTUs based on their relative abundances in each site. Clustering of Bray–Curtis distances matrix using the complete linkage method. The size of the circles indicates the repartition of a given OTU sequences among the four localities. The percentages indicate the OTUs’ proportions in the Spirochaeta dataset. Framed labels and black arrows indicate the selected OTUs that were selected to be process through the Minimum Decomposition Entropy pipeline (MED).

FIGURE 4

Median-joining oligotype networks of the three selected OTUs of Spirochaeta. Each circle represents a distinct oligotype. Colors indicate the locality of provenance. Circle size is scaled on the sum of the oligotype frequencies in each locality, within the corresponding OTU dataset. Raw abundances are provided in Supplementary File 2.

FIGURE 5

Gene flows summary and proposed dispersal routes across the Southern Ocean for each Spirochaeta taxa. Only the gene flows with Nm values > 0.25 are graphically represented. Discontinuous arrows represent Nm values > 0.25 and <1, continuous arrow represent Nm values > 1. Continuous arrows’ width is proportional to Nm values.