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.
Highlights
Biogeography has traditionally investigated the geographic distribution of macroorganisms in the Eukaryota domain
In the present proof-of-concept study, we aim to elucidate the evolutionary processes driving microbial biogeography across different provinces of the Southern Ocean (SO) by combining (1) communitywide surveying provided by the high-throughput sequencing of the 16S rRNA gene, (2) intra-species microdiversity resolution obtained through the oligotyping method implemented in the Minimum Entropy Decomposition” (MED) pipeline, and (3) phylogeographic analysis as traditionally developed for macroorganisms as models
Considering the SO as an outstanding idoneous frame, we investigated the geographic distribution of genetic diversity of marine bacterial taxa across three biogeographic provinces: maritime Antarctica (King George Island, South Shetland Islands, West Antarctic Peninsula), sub-Antarctic Islands of the Indian Ocean (Kerguelen archipelago), and southern South America (Patagonia)
Summary
Biogeography has traditionally investigated the geographic distribution of macroorganisms in the Eukaryota domain. Unlike contemporary driving factors (i.e., environmental selection) that have been extensively studied (Gilbert et al, 2012; Stegen et al, 2012; van der Gast, 2015), the role of historical processes – past ecological and evolutionary events – onto the present-day distribution patterns of microorganisms remains poorly investigated. The consensus was that the rapid and widespread dispersal of microbes should erase any signal of past historical events (Martiny et al, 2006). It is clear that historical processes, such as the dispersal barriers and geographic distance, might substantially contribute to microbes’ biogeography instead of environmental filtering (Hanson et al, 2012, 2019). Biogeographic regionalization, isolation, and endemism have been reported for microbes, reflecting the predominant effect of geographic distance over environmental variations (Papke et al, 2003; Whitaker et al, 2003)
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