Understanding the Mechanisms Behind the Response to Environmental Perturbation in Microbial Mats: A Metagenomic-Network Based Approach

Abstract

To date, it remains unclear how anthropogenic perturbations influence the dynamics of microbial communities, what general patterns arise in response to disturbance, and whether it is possible to predict them. Here, we suggest the use of microbial mats as a model of study to reveal patterns that can illuminate the ecological processes underlying microbial dynamics in response to stress. We traced the responses to anthropogenic perturbation caused by water depletion in microbial mats from Cuatro Cienegas Basin (CCB), Mexico, by using a time-series spatially resolved analysis in a novel combination of three computational approaches. First, we implemented MEBS (Multi-genomic Entropy-Based Score) to evaluate the dynamics of major biogeochemical cycles across spatio-temporal scales with a single informative value. Second, we used robust Time Series-Ecological Networks (TS-ENs) to evaluate the total percentage of interactions at different taxonomic levels. Lastly, we utilized network motifs to characterize specific interaction patterns. Our results indicate that microbial mats from CCB contain an enormous taxonomic diversity with at least 100 phyla, mainly represented by members of the rare biosphere (RB). Statistical ecological analyses point out a clear involvement of anaerobic guilds related to sulfur and methane cycles during wet versus dry conditions, where we find an increase in fungi, photosynthetic, and halotolerant taxa. TS-ENs indicate that in wet conditions, there was an equilibrium between cooperation and competition (positive and negative relationships, respectively), while under dry conditions there is an over-representation of negative relationships. Furthermore, most of the keystone taxa of the TS-ENs at family level are members of the RB and the microbial mat core highlighting their crucial role within the community. Our results indicate that microbial mats are more robust to perturbation due to redundant functions that are likely shared among community members in the highly connected TS-ENs with density values close to one (≈0.9). Finally, we provide evidence that suggests that a large taxonomic diversity where all community members interact with each other (low modularity), the presence of permanent of low-abundant taxa, and an increase in competition can be potential buffers against environmental disturbance in microbial mats.

Population genomics of Vibrionaceae isolated from an endangered oasis reveals local adaptation after an environmental perturbation.

“…We know by meteorological data that similar floods occur at CCB sporadically due to the low incidence of intense storms (i.e., only three since 1940 [49]). The flood introduced to this lowland a large amount of debris that, with time, generated an increase in nutrients, in particular phosphorus that in turn opened opportunities for the "rare biosphere", represented by standing bacterial lineages usually found at very low proportions, like the rare members of Vibrionaceae that normally are not common at the standard low nutrient conditions [50][51][52].…”

“…in CCB is needed. Unfortunately, this extraordinary oasis is disappearing, given the loss of more than 95% of CCB wetlands due to groundwater overexploitation by agriculture [27,47,52,65].…”

The lost world of Cuatro Ciénegas Basin, a relictual bacterial niche in a desert oasis

“…are competing actively in the microbial communities ( Pérez-Gutiérrez et al, 2013 ). Antagonisms and cooperation occur simultaneously in microbial mats and stromatolites ( Anda et al, 2018 ), and it is possible that the same dynamics occurred originally in the South-Western shores of Laurentia ( Kershaw, 2017 ).…”

Population genomics of Vibrionaceae isolated from an endangered oasis reveals local adaptation after an environmental perturbation

“…We know by meteorological data that similar floods occur at CCB sporadically, due to the low incidence of intense storms (i.e., three since 1940 [48]). The flood moved to this low land a large amount of debris that with time, generated an increase in nutrients, in particular phosphorus that opened opportunities for the “rare biosphere”, represented by standing bacterial lineages usually found at very low proportions, like the rare members of Vibrionaceae that normally are not common at standard low nutrient conditions [49–51]. Given this change in resources, we proposed two hypotheses when we started this study: Vibrionaceae from CCB would show as their ocean counterparts, an open pan-genome, showing high levels of recombination and genetic variation, as well as a high N e .…”

“…in CCB is needed. Unfortunately, this extraordinary oasis is disappearing, given the loss of more than 95% of CCB wetlands due to groundwater overexploitation by agriculture [27, 47,51, 64].…”