Interspecific interactions drive chitin and cellulose degradation by aquatic microorganisms

Abstract

Complex biopolymers (BPs) such as chitin and cellulose provide the majority of organic carbon in aquatic ecosystems, but the mechanisms by which communities of bacteria in natural systems exploit them are unclear. Previous degradation experiments in artificial systems predominantly used microcosms containing a single bacterial species, neglecting effects of interspecific interactions. By constructing simplified aquatic microbial communities, we tested how the addition of other bacterial species, of a nanoflagellate protist capable of consuming bacteria, or of both, affect utilization of BPs. Surprisingly, total abundance of resident bacteria in mixed communities increased upon addition of the protist. Concomitantly, bacteria shifted from free-living to aggregated morphotypes that seemed to promote utilization of BPs. In our model system, these interactions significantly increased productivity in terms of overall bacterial numbers and carbon transfer efficiency. This indicates that interactions on microbial aggregates may be crucial for chitin and cellulose degradation. We therefore suggest that interspecific microbial interactions must be considered when attempting to model the turnover of the vast pool of complex biopolymers in aquatic ecosystems.

Transparent exopolymer particles (TEP) are driven by chlorophyllaand mainly confined to the euphotic zone in a deep subalpine lake

“…factors, and general recirculation of nutrients in the microbial loop (Corno et al 2015). For example, in this study we did not consider the relative importance of grazing by heterotrophic nanoflagellates and zooplankton in disrupting or in promoting the formation of aggregates (Eckert et al 2013, Corno et al 2015, which can strongly impact the correlation between bacterial related variables and TEP.…”

Synergistic Interactions within a Multispecies Biofilm Enhance Individual Species Protection against Grazing by a Pelagic Protozoan

“…In the mixed-species consortia there was an increase by ∼2.5-fold in total bacterial cell numbers (all four species combined) in the grazed biofilm compared to the non-grazed biofilm, whereas in the planktonic fractions grazing reduced total cell numbers by ∼1.8-fold, emphasizing the protective nature of the biofilm mode of life. Evidence that grazing pressure is positively correlated with the formation of cell clusters has come from both monospecies laboratory biofilm ( Matz et al, 2004 , 2005 ) and from natural/semi-natural multispecies biofilm ( Wey et al, 2008 ; Rychert and Neu, 2010 ; Corno et al, 2015 ). Grazing induced biofilm formation could reflect either an active defense mechanism ( Matz and Kjelleberg, 2005 ; Friman and Buckling, 2014 ) or a passive mechanical process where the movement of the protozoan cells drives the bacterial cells to the substratum ( Wey et al, 2012 ).…”

“…Also, protozoan grazing on the planktonic bacterial population could release nutrients which stimulate the biofilm-associated cells resulting in enhanced levels of biofilm formation ( Petropoulos and Gilbride, 2005 ; Böhme et al, 2009 ). Additionally, the total bacterial productivity is shown to be influenced under grazing where bacterial aggregates display increased carbon transfer and uptake ( Corno et al, 2013 , 2015 ). Discrepancies found in the literature with respect to the protective nature of biofilms against grazing ( Jackson and Jones, 1991 ; Huws et al, 2005 ; Weitere et al, 2005 ) could be attributed to the type of protozoa used, their feeding mechanism and the growth conditions.…”

“…In multispecies biofilm settings, interactions between different bacteria play an important role in determining the structure, function and dynamics of the biofilms and it has been suggested that they contribute to defense mechanisms of bacterial biofilms against predators ( Wey et al, 2008 ; Matz, 2011 ). Moreover, it has been shown that interspecific interactions within the mixed bacterial communities in the presence of a grazing protist promoted co-aggregation of bacterial members and enhanced complex biopolymer degradation pathways leading to an overall increase in carbon transfer efficiency ( Corno et al, 2013 , 2015 ). Mixed biofilms have in other cases been shown to offer the harbored species protection against antibacterial compounds and enhanced capabilities of invasion and virulence within host organisms ( Burmølle et al, 2014 ).…”

Competition and niche separation of pelagic bacteria in freshwater habitats

“…It has been argued that the close physical associations between populations of attached microbes will strongly select for interaction‐driven community dynamics (Grossart et al ., ; Cordero and Datta, ), for example, with respect to communication (Gram et al ., ), metabolic complementarities (Beier and Bertilsson, ; Garcia et al ., ), parasitism (Jagmann et al ., ), or antagonism (Grossart et al ., ). In fact, the very formation of aggregates (Corno et al ., ) and the degradation of complex polymeric substrates (Beier and Bertilsson, ; Corno et al ., ) can be the result of cooperative interaction between species, resulting in reproducible succession patterns on aging particles (Datta et al ., ). Besides algal‐derived organic aggregates, freshwater microbes will also colonize other available surfaces, in particular the zooplankton (Tang et al ., ).…”