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Abstract
Lack of robustness is a major barrier to foster a sustainable cyanobacterial biotechnology. Use of cyanobacterial consortium increases biodiversity, which provides functional redundancy and prevents invading species from disrupting the production ecosystem. Here we characterized a cyanobacterial consortium enriched from microbial mats of alkaline soda lakes in BC, Canada, at high pH and alkalinity. This consortium has been grown in open laboratory culture for 4 years without crashes. Using shotgun metagenomic sequencing, 29 heterotrophic metagenome-assembled-genomes (MAGs) were retrieved and were assigned to Bacteroidota, Alphaproteobacteria, Gammaproteobacteria, Verrucomicrobiota, Patescibacteria, Planctomycetota, and Archaea. In combination with metaproteomics, the overall stability of the consortium was determined under different cultivation conditions. Genome information from each heterotrophic population was investigated for six ecological niches created by cyanobacterial metabolism and one niche for phototrophy. Genome-resolved metaproteomics with stable isotope probing using 13C-bicarbonate (protein/SIP) showed tight coupling of carbon transfer from cyanobacteria to the heterotrophic populations, specially Wenzhouxiangella. The community structure was compared to a previously described consortium of a closely related cyanobacteria, which indicated that the results may be generalized. Productivity losses associated with heterotrophic metabolism were relatively small compared to other losses during photosynthesis.
Highlights
Ecological interactions among phototrophs and heterotrophs are at the core of all light-exposed ecosystems and the entry into much of the biological carbon cycling on Earth (Paerl and Pinckney, 1996; Falkowski et al, 1998; Grossart et al, 2006; Azam and Malfatti, 2007)
From microbial mats growing in alkaline soda lakes located in BC, Canada (Sharp et al, 2017), a cyanobacterial consortium was enriched in a set of planar PBRs using medium “low-pH ammonium”
MetaErg was used for annotation of the MAGs (Dong and Strous, 2019). fastANI (Jain et al, 2018) was used for comparison of MAGs across samples to MAGs previously obtained from Kulunda soda lakes (Vavourakis et al, 2018) and Cariboo Plateau soda lakes (Zorz et al, 2019). 16S rRNA gene sequences were obtained with hyloFlash21 and were associated with MAGs based on phylogeny and sequencing coverage
Summary
Ecological interactions among phototrophs and heterotrophs are at the core of all light-exposed ecosystems and the entry into much of the biological carbon cycling on Earth (Paerl and Pinckney, 1996; Falkowski et al, 1998; Grossart et al, 2006; Azam and Malfatti, 2007). Highly productive cyanobacterial mats benefit from mutualistic phototroph–heterotroph interactions that are based on nutrient cycling (Christie-Oleza et al, 2017) These interactions occur in a context of recurring ecological niches, as shown by specific and conserved diurnal gene expression patterns of marine heterotrophs (Aylward et al, 2015). Overflow of fermentation products (Cano et al, 2018), release of osmolytes (Hagemann, 2011), and remains of dead cells (Aguilera et al, 2021) are examples of organic carbon produced by cyanobacteria that may remain unused These unused resources provide opportunities for successful invasion of cultivation systems, leading to a culture crash (Shelef and Soeder, 1980; Forehead and O’Kelly, 2013). The final DNA sample used was taken 1 year after the transfer to the stirred PBR
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