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

Abstract

Productivity is a major determinant of ecosystem diversity. Microbial ecosystems are the most diverse on the planet yet very few relationships between diversity and productivity have been reported as compared with macro-ecological studies. Here we evaluated the spatial relationships of productivity and microbiome diversity in a laboratory-cultivated photosynthetic mat. The goal was to determine how spatial diversification of microorganisms drives localized carbon and energy acquisition rates. We measured sub-millimeter depth profiles of net primary productivity and gross oxygenic photosynthesis in the context of the localized microenvironment and community structure, and observed negative correlations between species richness and productivity within the energy-replete, photic zone. Variations between localized community structures were associated with distinct taxa as well as environmental profiles describing a continuum of biological niches. Spatial regions in the photic zone corresponding to high primary productivity and photosynthesis rates had relatively low-species richness and high evenness. Hence, this system exhibited negative species-productivity and species-energy relationships. These negative relationships may be indicative of stratified, light-driven microbial ecosystems that are able to be the most productive with a relatively smaller, even distributions of species that specialize within photic zones.

Figure 1

The community and its environment. (a) Depth profile for the relative abundance of common taxa represented at the class level. (b) An excised microcosm of the benthic microbial ecosystem investigated. (c) Depth profile for spectral irradiance. (d) The dissolved O₂ profile. (e) The scalar irradiance (PAR) profile. (f) The porosity profile. Error bars represent ±1 s.d. from ⩾triplicate profile measurements. All depth profiles are reported as relative mat depth, which represents each position normalized by the total mat depth (1.05±0.4 cm). PAR, photosynthetically active radiation.

Figure 2

Heterogeneous depth profiles of productivity. (a) Net primary productivity as determined by ¹³C accumulation, denoted as %C replaced in the biomass pool over a 24 h incubation with labeled HCO₃⁻ (12:12 h, light: dark cycle); all data are plotted from three replicate profile measurements. (b) The gross rate of oxygenic photosynthesis; error bars represent ±1 s.d. from triplicate profile measurements. All depth profiles are reported as relative mat depth, which represents each position normalized by the total mat depth (1.05±0.4 cm).

Figure 3

Spatially resolved alpha diversity profiles. Species richness and evenness vary with: (a) relative mat depth; (b) the gross rate of oxygenic photosynthesis; (c) primary productivity; (d) porosity; (e) scalar irradiance (PAR); and (f) dissolved O₂. Linear regression was performed on rarefied samples corresponding to positions within the photic zone (yellow lines) and in the ‘dark' zone (gray lines). The shaded regions, around each line, represent ±1 s.e. PAR, photosynthetically active radiation.

Figure 4

Beta diversity. Canonical analysis of principal coordinates (CAP) of weighted UniFrac distances between rarified samples. These two principle components capture more than 55% of the variance observed. Each vector has a magnitude (length) sign (direction) of a variable's contributions to the principle components. Vectors represent: profiles for each measure of productivity (red), profiles of environmental properties (gray) and the most common taxa (blue). After merging OTUs at the family level, the ten most abundant families are shown here labeled at the family level (italics) or at a higher taxonomic level.