Morphogenesis and oxygen dynamics in phototrophic biofilms growing across a gradient of hydraulic conditions

Anna Depetris,Hannes Peter,Ankur Deep Bordoloi,Hippolyte Bernard,Amin Niayifar,Michael Kühl,Pietro De Anna,Tom Jan Battin

doi:10.1016/j.isci.2021.102067

Anna Depetris, Hannes Peter + Show 6 more

Open Access

https://doi.org/10.1016/j.isci.2021.102067

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Abstract

SummaryBiofilms are surface-attached and matrix-enclosed microbial communities that dominate microbial life in numerous ecosystems. Using flumes and automated optical coherence tomography, we studied the morphogenesis of phototrophic biofilms along a gradient of hydraulic conditions. Compact and coalescent biofilms formed under elevated bed shear stress, whereas protruding clusters separated by troughs formed under reduced shear stress. This morphological differentiation did not linearly follow the hydraulic gradient, but a break point emerged around a shear stress of ~0.08 Pa. While community composition did not differ between high and low shear environments, our results suggest that the morphological differentiation was linked to biomass displacement and reciprocal interactions between the biofilm structure and hydraulics. Mapping oxygen concentrations within and around biofilm structures, we provide empirical evidence for biofilm-induced alterations of oxygen mass transfer. Our findings suggest that architectural plasticity, efficient mass transfer, and resistance to shear stress contribute to the success of phototrophic biofilms.

Highlights

Microorganisms form surface-attached and matrix-enclosed biofilms in numerous ecosystems (Flemming and Wuertz, 2019)
Using flumes and automated optical coherence tomography, we studied the morphogenesis of phototrophic biofilms along a gradient of hydraulic conditions
We used an automated optical coherence tomography (OCT) system (Depetris et al, 2019) to characterize the biofilm surface topology at high resolution (40 mm, 40 mm, and 2.18 mm in x, y, z dimensions) across several spatial scales — ranging from patches formed by multicellular clusters (~100 mm) to the higher-order patterns emerging at the scale of the entire biofilm landscape (0.4 m in length) (Figures 1C–1G)

Summary

Introduction

Microorganisms form surface-attached and matrix-enclosed biofilms in numerous ecosystems (Flemming and Wuertz, 2019). A conspicuous and ubiquitous feature of biofilms is the differentiation into physical structures (i.e., architectures) and the formation of spatial patterns and stratifications at various scales. Despite the importance of spatial organization for ecological systems in general (Rietkerk, 2004), relatively little is known on the formation of the higher-order structures in complex biofilms. This is unexpected given that biofilm architecture seems to be related to critical processes in many benthic ecosystems (Battin et al, 2016; Findlay and Battin, 2016). Mechanical instabilities, reciprocal interactions between growth and competition for nutrients, localized cell death, and grazing by protists have been invoked as endogenous drivers of biofilm morphogenesis (Xavier et al, 2009; Yan et al, 2019; Dietrich et al, 2013; Weitere et al, 2018)

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