Metagenomic insight into taxonomic composition, environmental filtering, and functional redundancy for shaping worldwide modern microbial mats

Abstract

Although microbial mats are considered relictual communities that are nowadays mostly constrained in their distribution by predation and phosphorus availability, they are still found in a wide range of environmental conditions. Their ancestral history, geographical isolation, stratified community composition and interspecies dynamics make them an interesting model to study community ecological processes and concepts. In this study, we analyzed different metagenomic datasets from worldwide modern microbial mats to compare community structure and functions. We found significant differentiation in both alpha and beta diversity of taxonomic and functional categories without significant correlation with temperature and pH. Differences depended more on the presence of very highly abundant cyanobacteria and some generalist microorganisms. Our results suggest that there is more than just Grinnellian niche dynamics in the determination of microbial mat community assembly, opening the hypothesis of interactions as the driver behind these ancient communities. We also discuss the influence of niche dynamics and environmental filtering in the community assembly of microbial mats.

Divide and conquer: Spatial and temporal resource partitioning structures benthic cyanobacterial mats

“…Maintenance of functional diversity is upheld by functional redundancy, which is a common theme in mats across environments (Nemergut et al, 2013). Viladomat et al (2022) used metagenomic datasets to show how functional redundancy was common in BCMs, and mats maintained the same physiological cycles despite the specific species involved. This functional redundancy makes mats resilient to perturbations and allows for maintenance of BCM community stability across desiccation and subsequent rewetting in stream beds, which has been observed to result in higher cooperation under wet conditions (de Anda et al, 2018).…”

“…Overall, carbon and oxygen produced and fixed by photosynthesizing mat members create and sustain oxic gradients that affect the microbes around them. Once these gradients are set in place, they are often self‐reinforcing: resource partitioning of photosynthetically fixed carbon and oxygen helps perpetuate necessary environmental gradients (Canfield & Des Marais, 1993; Hubas et al., 2017; Meier et al., 2021; Viladomat et al., 2022). Analyzing how biogeochemical cycling within mats affects not only the mats, but also the surrounding water column and ecosystem is critical, as carbon release from BCMs has been determined to be a significant contributor to tropical reef carbon cycling and microbialization (Brocke et al., 2015; Haas et al., 2016; Mueller et al., 2022).…”

“…Where initial populations of microbes that form BCMs come from is a topic of great importance but with little concrete supporting evidence. Some authors have suggested potential “seed populations” of bacteria within sediments or the water column that could be feeding proliferation, given the right environmental conditions (Nemergut et al., 2013; Viladomat et al., 2022). Others describe fish feeding on BCMs (Cissell et al., 2019; Manning & McCoy, 2023), which may act as a vector for mat proliferation and range expansion via their excrement, since cyanobacteria can survive passage through fish guts (Cissell & McCoy, 2023a; Lewin et al., 2003).…”

“…It is also important to consider the effects of unstable coexistence and functional redundancy in BCM communities. Benthic cyanobacterial mats have high diversity and often high functional redundancy (de Anda et al., 2018; Viladomat et al., 2022). Indeed, coexistence is continuously mediated by species turnover within a system and is often facilitated by disturbance (Chesson, 2000; Connell, 1978).…”

“…In the past, the main focus of BCM studies was on descriptive studies that examined bacterial diversity within mats, and only more recently have mechanistic studies on the functional capabilities of BCM microbial members begun to be explored (Cissell & McCoy, 2021; Fan et al., 2015b; Grim et al., 2021; Lee et al., 2018; Mobberley et al., 2017; Woebken et al., 2015). As metagenomic and transcriptomic sequencing have become less costly, these techniques have also recently been utilized in BCMs, allowing for deeper understanding of fine‐scale resource partitioning and spatial and temporal differences that influence and are influenced by the microbial composition (e.g., Cissell & McCoy, 2021; Nemergut et al., 2013; Varin et al., 2010; Viladomat et al., 2022). Here, we present an updated review on BCM communities and their biogeochemical cycling through a niche partitioning lens, linking spatial and temporal resource partitioning to functional nutrient cycling processes that affect mat proliferation across environments.…”