Incipient Sympatric Speciation and Evolution of Soil Bacteria Revealed by Metagenomic and Structured Non-Coding RNAs Analysis

Abstract

Soil bacteria respond rapidly to changes in new environmental conditions. For adaptation to the new environment, they could mutate their genome, which impacts the alternation of the functional and regulatory landscape. Sometimes, these genetic and ecological changes may drive the bacterial evolution and sympatric speciation. Although sympatric speciation has been controversial since Darwin suggested it in 1859, there are several strong theoretical or empirical evidences to support it. Sympatric speciation associated with soil bacteria remains largely unexplored. Here, we provide potential evidence of sympatric speciation of soil bacteria by comparison of metagenomics from two sharply contrasting abutting divergence rock and soil types (Senonian chalk and its rendzina soil, and abutting Pleistocene basalt rock and basalt soil). We identified several bacterial species with significant genetic differences in the same species between the two soil types and ecologies. We show that the bacterial community composition has significantly diverged between the two soils; correspondingly, their functions were differentiated in order to adapt to the local ecological stresses. The ecologies, such as water availability and pH value, shaped the adaptation and speciation of soil bacteria revealed by the clear-cut genetic divergence. Furthermore, by a novel analysis scheme of riboswitches, we highlight significant differences in structured non-coding RNAs between the soil bacteria from two divergence soil types, which could be an important driver for functional adaptation. Our study provides new insight into the evolutionary divergence and incipient sympatric speciation of soil bacteria under microclimatic ecological differences.

Host diet shapes functionally differentiated gut microbiomes in sympatric speciation of blind mole rats in Upper Galilee, Israel

“…The divergence of soil microbiome between the chalk and basalt is larger than gut microbiome. At the species level (Mukherjee et al, 2022), we found that the soil bacteria differentiation between basalt and chalk is larger than that of the same species in the gut (Figure 4D), which may be due to a combination of more contrasting edaphic stresses and longer divergence time of the soil microbiome. The divergence of the soil microbiome started when volcanic eruptions formed new habitats 1 million years ago, but the hosts of blind mole rats split much later only 0.228 Mya which hampered the gut microbial divergence (Supplementary Figure 4).…”

“…The ancestral chalk species is from Senonian, while the basalt species is from a volcanic eruption during the Quaternary, which is like basalt islands floating on chalk ocean ( Figure 1B ; Segev et al, 2002 ). When the volcano initially erupted about 1 million years ago and cooled down, new vegetation ( Hadid et al, 2013 ), food resources ( Figures 1C , 2C ), and ecological niches ( Figure 1B ) emerged, allowing animals to immigrate from the ancestral chalk to the new derivative symparic species on the basalt, forming the new species on the basalt ( Hadid et al, 2013 ; Nevo, 2013 ; Singaravelan et al, 2013 ; Li K. et al, 2015 ; Lövy et al, 2015 , 2017 , 2020 ; Li et al, 2016 , 2020a , b ; Šklíba et al, 2016 ; Jiao et al, 2021 ; Mukherjee et al, 2022 ; Nevo and Li, 2022 ; Figures 1A , 2C ). This provided us with an ideal model to further understand the complex interaction of the gut microbiome, the host, and its corresponding environment.…”

“…Basically, the same species or similar species compositions in the gut microbiome of blind mole rats can perform different functions, which was consistent with our finding of differentiation of the probably same species between the two types of environments ( Figure 4 ; Supplementary Figures 12 – 31 ). The microbe from the two contrasting soils was significantly different in both community composition and function ( Mukherjee et al, 2022 ). The divergence of the gut microbiome was significantly smaller than that of the soil microbiome ( Figure 4 ); this is likely because the soil difference is larger than that of the gut environment.…”

“…The community composition between the chalk and basalt gut microbiome was not significantly different (Supplementary Figure 4) when compared to its host phylogeny (Figure 1D), host diet (Figure 2) or the environmental soil metagenomes (Mukherjee et al, 2022), which may be due to the fact that divergence between the chalk and basalt microbiome occurred much later (Li K. et al, 2015). However, the main question still stands: which environmental factor is the main driver of the microbial divergence between the chalk and basalt, or have all of them shaped the gut microbiome together?…”

“…Paired-end raw sequencing reads were first trimmed by SOAPnuke ( Chen Y. et al, 2018 ) to remove adapters and low-quality bases, and the host reads ( S. galili ) were removed by SOAPaligner ( Li R. et al, 2009 ). We also collected 12 soil samples for shotgun metagenomic sequencing at the same location ( Mukherjee et al, 2022 ), and the data of soil were processed as described below.…”