Organic Electron Donors and Terminal Electron Acceptors Structure Anaerobic Microbial Communities and Interactions in a Permanently Stratified Sulfidic Lake.

Connie A Rojas,Serry Park,Vanja Klepac-Ceraj,Tanja Bosak,Ana De Santiago Torio

doi:10.3389/fmicb.2021.620424

Abstract

The extent to which nutrients structure microbial communities in permanently stratified lakes is not well understood. This study characterized microbial communities from the anoxic layers of the meromictic and sulfidic Fayetteville Green Lake (FGL), NY, United States, and investigated the roles of organic electron donors and terminal electron acceptors in shaping microbial community structure and interactions. Bacterial communities from the permanently stratified layer below the chemocline (monimolimnion) and from enrichment cultures inoculated by lake sediments were analyzed using 16S rRNA gene sequencing. Results showed that anoxygenic phototrophs dominated microbial communities in the upper monimolimnion (21 m), which harbored little diversity, whereas the most diverse communities resided at the bottom of the lake (∼52 m). Organic electron donors explained 54% of the variation in the microbial community structure in aphotic cultures enriched on an array of organic electron donors and different inorganic electron acceptors. Electron acceptors only explained 10% of the variation, but were stronger drivers of community assembly in enrichment cultures supplemented with acetate or butyrate compared to the cultures amended by chitin, lignin or cellulose. We identified a range of habitat generalists and habitat specialists in both the water column and enrichment samples using Levin’s index. Network analyses of interactions among microbial groups revealed Chlorobi and sulfate reducers as central to microbial interactions in the upper monimolimnion, while Syntrophaceae and other fermenting organisms were more important in the lower monimolimnion. The presence of photosynthetic microbes and communities that degrade chitin and cellulose far below the chemocline supported the downward transport of microbes, organic matter and oxidants from the surface and the chemocline. Collectively, our data suggest niche partitioning of bacterial communities via interactions that depend on the availability of different organic electron donors and terminal electron acceptors. Thus, light, as well as the diversity and availability of chemical resources drive community structure and function in FGL, and likely in other stratified, meromictic lakes.

Highlights

We use a combination of 16S rRNA gene sequencing, enrichment cultures and network analyses to: (1) characterize the composition and diversity of bacterial communities below the chemocline in Fayetteville Green Lake (FGL); (2) determine how organic electron donors and terminal electron acceptors drive microbial community structure and function below the photic zone; and (3) elucidate key microbial interactions potentially involved in nutrient cycling
Rarefaction analysis indicated that the depths from the upper monimolimnion were more completely sampled than the deeper depths (Supplementary Figure 1)
The primer bias against Archaea is known (Pinto and Raskin, 2012), these values closely resembled the values observed in the FGL metagenome data generated to check for the primer bias in the 16S rRNA amplicon data

Summary

INTRODUCTION

Microbial communities in permanently stratified ecosystems, such as sulfidic meromictic lakes, mediate the biogeochemical cycling of carbon, oxygen, sulfur, and other elements (Bosshard et al, 2000; Lehours et al, 2005, 2007; Lauro et al, 2011; Comeau et al, 2012; Baricz et al, 2014; Andrei et al, 2015; Baatar et al, 2016; Meyerhof et al, 2016). We use a combination of 16S rRNA gene sequencing, enrichment cultures and network analyses to: (1) characterize the composition and diversity of bacterial communities below the chemocline in FGL; (2) determine how organic electron donors and terminal electron acceptors drive microbial community structure and function below the photic zone; and (3) elucidate key microbial interactions potentially involved in nutrient cycling. Comparisons of the 16S rRNA gene surveys of microbial communities sampled from different depths of the lake along with those obtained under a range of culturing conditions reveal specific microbe-microbe interactions that may couple and mediate the biogeochemical cycling of carbon and other elements in meromictic lakes. Elemental sulfur (MW = 32.08 g/mol) was heat sterilized at 110◦C overnight and added to a bottle containing FGL medium to generate a ∼1 M stock solution This solution was mixed by shaking and used in the enrichments at the final concentration of ∼10 mM. Raw metagenome sequence files and contigs are available upon request

RESULTS

DISCUSSION

DATA AVAILABILITY STATEMENT