The effect of carbon subsidies on marine planktonic niche partitioning and recruitment during biofilm assembly

Chuck Pepe-Ranney, Edward Hall

Abstract

Introduction

Biofilms are diverse and complex microbial consortia, and, the biofilm lifestyle is the rule rather than the exception for microbes in many environments. Large and small-scale biofilm architectural features play an important role in their ecology and influence their role in biogeochemical cycles (Battin et al., 2007). Fluid mechanics impact biofilm structure and assembly (Hodl et al., 2011; Besemer et al., 2009; Battin et al., 2003), but it is less clear how other abiotic factors such as resource availability affect biofilm assembly. Aquatic biofilms initiate with seed propagules from the planktonic community (Hodl et al., 2011; McDougald et al., 2011). Thus, resource amendments that influence planktonic communities may also influence the recruitment of microbial populations during biofilm community assembly.

In a crude sense, biofilm and planktonic microbial communities divide into two key groups: oxygenic phototrophs including eukaryotes and cyanobacteria (hereafter “photoautotrophs”), and heterotrophic bacteria and archaea. This dichotomy, admittedly an abstraction (e.g. non-phototrophs can also be autotrophs), can be a powerful paradigm for understanding community shifts across ecosystems of varying trophic state (Cotner et al., 2002). Heterotrophs meet some to all of their organic carbon (C) requirements from photoautotroph produced C while simultaneously competing with photoautotrophs for limiting nutrients such as phosphorous (P) (Bratbak et al., 1985). The presence of external C inputs, such as terrigenous C leaching from the watershed (Jansson et al., 2008; Karlsson et al., 2012) or C exudates derived from macrophytes (Stets et al., 2008a; Stets et al., 2008b), can alleviate heterotroph reliance on photoautotroph derived C and shift the heterotroph-photoautotroph relationship from commensal and competitive to strictly competitive . Therefore, increased C supply should increase the resource space available to heterotrophs and increase competition for mineral nutrients decreasing nutrients available for photoautotrophs (assuming that heterotrophs are superior competitors for limiting nutrients as has been observed ). These dynamics should result in the increase in heterotroph biomass relative to the photoautotroph biomass along a gradient of increasing labile C inputs. We refer to this differential allocation of limiting resources among components of the microbial community as niche partitioning.

While these gross level dynamics have been discussed conceptually (Cotner et al., 2002) and to some extent demonstrated empirically (Stets et al., 2008a), the effects of biomass dynamics on photoautotroph and heterotroph membership and structure has not been directly evaluated in plankton or biofilms. In addition, how changes in planktonic communities propagate to biofilms during community assembly is not well understood. We designed this study to test if C subsidies shift the biomass balance between autotrophs and heterotrophs within the biofilm or its seed pool (i.e. the plankton), and, to measure how changes in biomass pool size alter composition of the plankton and biofilm communities. Specifically, we amended marine mesocosms with varying levels of labile C input and evaluated differences in photoautotroph and heterotrophic bacterial biomass in plankton and biofilm samples along the C gradient. In each treatment we characterized plankton and biofilm community composition by PCR amplifying and DNA sequencing 16S rRNA genes and plastid 23S rRNA genes.