Trophic interactions shape the spatial organization of medium-chain carboxylic acid producing granular biofilm communities

Candry, Pieter; Chadwick, Grayson L.; Caravajal-Arroyo, José Maria; Lacoere, Tim; Winkler, Mari-Karoliina Henriikka; Ganigué, Ramon; Orphan, Victoria J.; Rabaey, Korneel

doi:10.1038/s41396-023-01508-8

Trophic interactions shape the spatial organization of medium-chain carboxylic acid producing granular biofilm communities

Journal Article · Fri Sep 15 00:00:00 EDT 2023 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-023-01508-8· OSTI ID:2280752

; Chadwick, Grayson L.; Caravajal-Arroyo, José Maria; Lacoere, Tim; Winkler, Mari-Karoliina Henriikka; ; ;

Abstract

Granular biofilms producing medium-chain carboxylic acids (MCCA) from carbohydrate-rich industrial feedstocks harbor highly streamlined communities converting sugars to MCCA either directly or via lactic acid as intermediate. We investigated the spatial organization and growth activity patterns of MCCA producing granular biofilms grown on an industrial side stream to test (i) whether key functional guilds (lactic acid producing Olsenella and MCCA producing Oscillospiraceae) stratified in the biofilm based on substrate usage, and (ii) whether spatial patterns of growth activity shaped the unique, lenticular morphology of these biofilms. First, three novel isolates (one Olsenella and two Oscillospiraceae species) representing over half of the granular biofilm community were obtained and used to develop FISH probes, revealing that key functional guilds were not stratified. Instead, the outer 150–500 µm of the granular biofilm consisted of a well-mixed community of Olsenella and Oscillospiraceae, while deeper layers were made up of other bacteria with lower activities. Second, nanoSIMS analysis of 15N incorporation in biofilms grown in normal and lactic acid amended conditions suggested Oscillospiraceae switched from sugars to lactic acid as substrate. This suggests competitive-cooperative interactions may govern the spatial organization of these biofilms, and suggests that optimizing biofilm size may be a suitable process engineering strategy. Third, growth activities were similar in the polar and equatorial biofilm peripheries, leaving the mechanism behind the lenticular biofilm morphology unexplained. Physical processes (e.g., shear hydrodynamics, biofilm life cycles) may have contributed to lenticular biofilm development. Together, this study develops an ecological framework of MCCA-producing granular biofilms that informs bioprocess development.

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Research Organization:: University of Washington, Seattle, WA (United States)

Sponsoring Organization:: Simons Foundation; USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0020356; SC0020373

OSTI ID:: 2280752

Alternate ID(s):: OSTI ID: 2229837

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 11 Vol. 17; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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