Phototrophic biofilm assembly in microbial-mat-derived unicyanobacterial consortia: model systems for the study of autotroph-heterotroph interactions

Abstract

Microbial autotroph-heterotroph interactions influence biogeochemical cycles on a global scale, but the diversity and complexity of natural systems and their intractability to in situ manipulation make it challenging to elucidate the principles governing these interactions. The study of assembling phototrophic biofilm communities provides a robust means to identify such interactions and evaluate their contributions to the recruitment and maintenance of phylogenetic and functional diversity over time. To examine primary succession in phototrophic communities, we isolated two unicyanobacterial consortia from the microbial mat in Hot Lake, Washington, characterizing the membership and metabolic function of each consortium. We then analyzed the spatial structures and quantified the community compositions of their assembling biofilms. The consortia retained the same suite of heterotrophic species, identified as abundant members of the mat and assigned to Alphaproteobacteria, Gammaproteobacteria, and Bacteroidetes. Autotroph growth rates dominated early in assembly, yielding to increasing heterotroph growth rates late in succession. The two consortia exhibited similar assembly patterns, with increasing relative abundances of members from Bacteroidetes and Alphaproteobacteria concurrent with decreasing relative abundances of those from Gammaproteobacteria. Despite these similarities at higher taxonomic levels, the relative abundances of individual heterotrophic species were substantially different in the developing consortial biofilms. This suggests that, although similar niches are created by the cyanobacterial metabolisms, the resulting webs of autotroph-heterotroph and heterotroph-heterotroph interactions are specific to each primary producer. The relative simplicity and tractability of the Hot Lake unicyanobacterial consortia make them useful model systems for deciphering interspecies interactions and assembly principles relevant to natural microbial communities.

Trade-offs between microbiome diversity and productivity in a stratified microbial mat

“…Interestingly, this cyanobacterium is known to be motile and metabolically coupled to heterotrophic bacteria that match or are very similar to the OTUs abundant near the surface of the mat, for example, Roseibacterium sp. HL7711_P4H5 (Cole et al, 2014;Nelson et al, 2016). The most abundant OTU identified in this system belonged to a cyanobacterium of the family Pseudanabaenaceae.…”

“…These niche spaces mapped to common taxa that were associated with measured variance in community structure (beta diversity shown in Figure 4). Some OTUs, belonging to the most abundant families (Supplementary Figure S5), matched species that have been previously described and sequenced (Cole et al, 2014;Nelson et al, 2016) allowing function, relating to microbial lifestyle and niche space, to be inferred. The Phormidium sp.…”

“…Reads from family Phormidiaceae were dominated by an OTU that exhibited 100% identity to previously identified filamentous cyanobacterium Phormidium sp. OSCR, cultivated within a consortium from the Hot Lake mat (Cole et al, 2014). Rhodobacteraceae and the ML635J-40 family of the order Bacteroidales also varied in the same direction as productivity.…”

“…An abundant member in family Rhodobacteraceae was an identical match to a previously described Roseibacterium sp. HL7711_P4H5, also a member of the Hot Lake unicyanobacterial consortia (Cole et al, 2014).…”

Next‐generation studies of microbial biofilm communities

“…Further, we and others have observed that such mixed communities have heightened tolerance to antimicrobials, chemical stress and predation (Burmolle et al ., 2006; Lee et al ., 2014; Kumar and Ting, 2015). Additional models allow for studies of autotroph–heterotroph interactions (Elenter et al ., 2007; Cole et al ., 2014), metabolic cooperation to degrade xenobiotics (Christensen et al ., 2002) and cooperation and competition between different species (Foster and Bell, 2012; Fiegna et al ., 2015), as examples of biofilm community interactions recently explored.…”