AUTHOR=Brileya Kristen A. , Camilleri Laura B. , Zane Grant M. , Wall Judy D. , Fields Matthew W. 

TITLE=Biofilm growth mode promotes maximum carrying capacity and community stability during product inhibition syntrophy

JOURNAL=Frontiers in Microbiology

VOLUME=5

YEAR=2014

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2014.00693

DOI=10.3389/fmicb.2014.00693

ISSN=1664-302X

ABSTRACT=<p>Sulfate-reducing bacteria (SRB) can interact syntrophically with other community members in the absence of sulfate, and interactions with hydrogen-consuming methanogens are beneficial when these archaea consume potentially inhibitory H<sub>2</sub> produced by the SRB. A dual continuous culture approach was used to characterize population structure within a syntrophic biofilm formed by the SRB <italic>Desulfovibrio vulgaris</italic> Hildenborough and the methanogenic archaeum <italic>Methanococcus maripaludis</italic>. Under the tested conditions, monocultures of <italic>D. vulgaris</italic> formed thin, stable biofilms, but monoculture <italic>M. maripaludis</italic> did not. Microscopy of intact syntrophic biofilm confirmed that <italic>D. vulgaris</italic> formed a scaffold for the biofilm, while intermediate and steady-state images revealed that <italic>M. maripaludis</italic> joined the biofilm later, likely in response to H<sub>2</sub> produced by the SRB. Close interactions in structured biofilm allowed efficient transfer of H<sub>2</sub> to <italic>M. maripaludis,</italic> and H<sub>2</sub> was only detected in cocultures with a mutant SRB that was deficient in biofilm formation (Δ<italic>pilA</italic>). <italic>M. maripaludis</italic> produced more carbohydrate (uronic acid, hexose, and pentose) as a monoculture compared to total coculture biofilm, and this suggested an altered carbon flux during syntrophy. The syntrophic biofilm was structured into ridges (∼300 × 50 μm) and models predicted lactate limitation at ∼50 μm biofilm depth. The biofilm had structure that likely facilitated mass transfer of H<sub>2</sub> and lactate, yet maximized biomass with a more even population composition (number of each organism) when compared to the bulk-phase community. Total biomass protein was equivalent in lactate-limited and lactate-excess conditions when a biofilm was present, but in the absence of biofilm, total biomass protein was significantly reduced. The results suggest that multispecies biofilms create an environment conducive to resource sharing, resulting in increased biomass retention, or carrying capacity, for cooperative populations.</p>