Biology subjects

Battin, T. J.

Publications and source records attributed to Battin, T. J..

6 recordsLinked to original sources

bioRxiv2026

Evolutionary radiation of Polaromonas from mountain glaciers downstream

Habitat transitions are central to microbial ecology and evolution and have been extensively studied across vastly different environments, such as between saline and non-saline environments. However, microbial habitat transitions along other large-scale environmental gradients remain poorly studied. This is particularly true for transitions involving the cryosphere, despite building evidence suggesting the Cryogenian as important for evolutionary radiation. Here, we investigated ecosystem transitions and related genomic adaptations of the cosmopolitan cryospheric Polaromonas bacterium. We constructed a pangenome from 282 high-quality genomes, sourced from glaciers, glacier-fed streams, lakes, wetlands, groundwater, rivers, and soils. Phylogenetic reconciliation revealed that the ancestral Polaromonas genome radiated from glacier ecosystems into various downstream environments through multiple independent transitions. These transitions were marked by extensive horizontal gene transfer and gene loss, with mobile genetic elements, such as plasmids and prophages playing key roles in genomic diversification. Predicted ancestral genomes encoded versatile metabolic and stress-response capacities, supporting adaptation to fluctuating and extreme conditions in the various cryospheric habitats. Compared to the ancestral Polaromonas genome, distinct genomic signatures were associated with specific habitats: glacier-fed stream lineages possess expanded stress tolerance repertoires, glacier lineages gained chemolithotrophic and anaerobic pathways, lake and wetland genomes acquired phototrophic functions, and soil lineages expanded substrate transport and stress tolerance. Together, our findings highlight the role of genomic plasticity in the ecological success of Polaromonas, and also underscore the cryosphere as a potential evolutionary cradle from which lineages dispersed and adapted to downstream aquatic and terrestrial environments.

microbiology↗

bioRxiv2023

The role of phages in proglacial stream biofilm communities characterized by microdiversity

Viruses modulate the diversity and activity of microbial communities. However, little is known about their role for the structure of stream biofilms communities. Here, we present insights into the diversity and composition of viral communities in various streams draining three proglacial floodplains in Switzerland. Proglacial streams are characterized by extreme environmental conditions, including near-freezing temperatures and ultra-oligotrophy. These conditions select for few but well-adapted bacterial clades, which dominate biofilm communities and occupy niches via microdiversification. We used metagenomic sequencing to reveal a remarkably diverse biofilm virome in these streams. Across the different floodplains and streams, viral community composition was tightly coupled to that of the bacterial hosts, which was underscored by generally high host specificity. Combining predictions of phage-host interactions with auxiliary metabolic genes (AMGs), we identify specific AMGs shared by phages infecting microdiverse clade members. Our work provides a step towards a better understanding of the complex interactions among bacteria and phages in stream biofilm communities in general and streams influenced by glacier meltwaters and characterized by microdiversity in particular.

ecology↗

bioRxiv2023

Bacteroides thetaiotaomicron metabolic activity decreases with polysaccharide molecular weight

The human colon hosts hundreds of commensal bacterial species, many of which ferment complex dietary carbohydrates. To transform these fibers into metabolically-accessible compounds, microbes often express series of dedicated enzymes homologous to the starch utilization system (sus) encoded in polysaccharide utilization loci (PULs). The genome of Bacteroides thetaiotaomicron (Bt), a common member of the human gut microbiota, encodes nearly 100 PULs, conferring a strong metabolic versatility. While the structures and functions of individual enzymes within the PULs have been investigated, little is known about how polysaccharide complexity impacts the function of sus-like systems. We here show that the activity of sus-like systems depends on polysaccharide size, ultimately impacting bacterial growth. We demonstrate the effect of size-dependent metabolism in the context of dextran metabolism driven by the specific utilization system PUL48. We find that as molecular weight of dextran increases, Bt growth rate decreases and lag time increases. At the enzymatic level, the dextranase BT3087 is the main glycosylhydrolase for dextran utilization and that BT3087 and BT3088 contribute to Bt dextran metabolism in a size-dependent manner. Finally, we show that the polysaccharide size-dependent metabolism of Bt impacts its metabolic output in a way that modulates the composition of a producer-consumer community it forms with Bacteroides fragilis. Altogether, our results expose an overlooked aspect of Bt metabolism which can impact the composition and diversity of microbiota.

microbiology↗

bioRxiv2022

Fluid flow structures gut microbiota biofilm communities by distributing public goods

Bacterial gut commensals experience a biologically and physically complex mucosal environment. While many chemical factors mediate the composition and structure of these microbial communities, less is known about the role of mechanics. Here, we demonstrate that fluid flow impacts the spatial organization and composition of gut biofilm communities by shaping how different species interact metabolically. We first demonstrate that a model community composed of Bacteroides thetaiotaomicron (Bt) and Bacteroides fragilis (Bf), two representative human commensals, can form robust biofilms in flow. We identified dextran as a polysaccharide readily metabolized by Bt but not Bf, but whose fermentation generates a public good enabling Bf growth. We demonstrate that in flow, Bt biofilms share dextran metabolic by-products, promoting Bf biofilm formation. By transporting this public good, flow structures the spatial organization of the community, positioning the Bf population downstream from Bt. We show that sufficiently strong flows abolish Bf biofilm formation by limiting the effective public good concentration at the surface. Physical factors such as flow may therefore contribute to the composition of intestinal microbial communities, potentially impacting host health.

microbiology↗

bioRxiv2021

Genomic and metabolic adaptations of biofilms to ecological windows of opportunities in glacier-fed streams

Microorganisms dominate life in cryospheric ecosystems. In glacier-fed streams (GFSs), ecological windows of opportunities allow complex microbial biofilms to develop and transiently form the basis of the food web, thereby controlling key ecosystem processes. Here, using high-resolution metagenomics, we unravel strategies that allow biofilms to seize this opportunity in an ecosystem otherwise characterized by harsh environmental conditions. We found a diverse microbiome spanning the entire tree of life and including a rich virome. Various and co-existing energy acquisition pathways point to diverse niches and the simultaneous exploitation of available resources, likely fostering the establishment of complex biofilms in GFSs during windows of opportunity. The wide occurrence of rhodopsins across metagenome-assembled genomes (MAGs), besides chlorophyll, highlights the role of solar energy capture in these biofilms. Concomitantly, internal carbon and nutrient cycling between photoautotrophs and heterotrophs may help overcome constraints imposed by the high oligotrophy in GFSs. MAGs also revealed mechanisms potentially protecting bacteria against low temperatures and high UV-radiation. The selective pressure of the GFS environment is further highlighted by the phylogenomic analysis, differentiating the representatives of the genus Polaromonas, an important component of the GFS microbiome, from those found in other ecosystems. Our findings reveal key genomic underpinnings of adaptive traits that contribute to the success of complex biofilms to exploit environmental opportunities in GFSs, now rapidly changing owing to global warming.

microbiology↗

bioRxiv2020

Homogeneous selection promotes microdiversity in the glacier-fed stream microbiome

Microdiversity, the organization of microorganisms into groups with closely related but ecologically different sub-types, is widespread and represents an important linchpin between microbial ecology and evolution. However, the drivers of microdiversification remain largely unknown. Here we show that selection promotes microdiversity in the microbiome associated with sediments in glacier-fed streams (GFS). Applying a novel phylogenetic framework, we identify several clades that are under homogeneous selection and that contain genera with higher levels of microdiversity than the rest of the genera. Overall these clades constituted [~]44% and [~]64% of community -diversity and abundance, and both percentages increased further in GFS that were largely devoid of primary producers. Our findings show that strong homogeneous selection drives the microdiversification of specialized microbial groups putatively underlying their success in the extreme environment of GFS. This microdiversity could be threatened as glaciers shrink, with unknown consequences for microbial diversity and functionality in these ecosystems.

ecology↗