Aarhus Universitets segl

Community and control of filamentous sulfur bacteria

Publikation: Bog/antologi/afhandling/rapportPh.d.-afhandling

Bacterial communities in sediment are driven by several factors, including the availability of electron donors and acceptors such as sulfur, oxygen, and organic matter, as well as sedimentological and geochemical properties. In addition, biotic factors such as bacteriophage predation also play an essential role in shaping these communities and impacting biochemical cycles. Sediments with high loads of organic matter harbor bacteria harnessing organic and inorganic carbon sources and other inorganic energy sources, like sulfide and H2, through alternative electron acceptors, such as sulfate and nitrate. In this scenery, large filamentous multicellular bacteria doing sulfide oxidation using alternative electron acceptors and oxygen, when available, are conspicuous inhabitants of benthic bacterial mats. Indeed, forms from Gammaproteobacteria: Thioploca, Beggiatoa, and the spherical Thiomargarita are usual inhabitants of organic matter-rich and sulfidic sediments in different locations in the world. For example, in the so-called Humboldt Sulfuretum (HS) biome, on the north-central Chilean coast, vast bacterial mats have been reported for decades, mainly compounded by Thioploca spp., such as the proposed Candidatus Marithioploca. In addition, large filamentous bacteria include other taxonomic representatives with different metabolic strategies in the Chloroflexi, Firmicutes and Desulfobacterota. One unique sulfide-oxidizing large filamentous multicellular bacteria is the so-called cable bacteria (CB), which facilitates long-distance electron transport (LDET) over centimeter distances, thus coupling sulfide oxidation in deeper sediment layers with the O2 or nitrate reduction near the sediment interface.
While the ecology and physiology of sediment-dwelling bacterial communities, particularly large filamentous bacteria, have been investigated for decades, their relationship to bacteriophages (virus-infecting bacteria), phages for short, has not been thoroughly studied. In this sense, phages are critical players in all environments, especially in marine sediments, where their abundance is more significant than in any other setting. In this sense, phages modulate bacterial populations, infecting and killing them. However, phages also play an essential role in transferring genes and new traits to their host through the lysogenic cycle; temperate phages integrate their genome into the host.
This thesis investigated the diversity and structure of bacterial communities in sediment environments, focusing on hypoxic-anoxic sediments, large filamentous multicellular bacteria, and cable bacteria as a virus-related case study. Thus, firstly, through 16S rDNA gene amplicons, I elucidated the diversity and structure of the HS bacterial community. Surprisingly, Desulfobulbaceae, which contains the genera Ca. Electrothrhix, Desulfobulbacea, and
undescribed forms are crucial in the biogeographic pattern. Furthermore, the microdiversity is very high, and only a small part of the taxonomic entities, amplicon sequence variants (ASVs), are shared in the whole system. In addition, the most abundant bacteria were those related to sulfur and H2 metabolism and the taxonomic branches that contain large filamentous bacteria. Thus, in the second part of this thesis, I investigated fifteen large filamentous bacteria isolated directly from HS sediment samples using microcapillaries through a micromanipulator device, allowing the selection of different individual morphotypes. Following DNA extraction and genome amplifications, whole genome sequencing, and bioinformatics processing, new species in Thiotrichales, Desulfobacterales, Chloroflexi, and Firmicutes, with different metabolic strategies, were revealed. Interestingly, these large bacteria harbor diverse defense systems and prophages, suggesting frequent and intense interaction with phages.
Considering the latest information on the relationship of large filamentous multicellular bacteria to viruses and the previous report on CB population collapse and phage traces in their genomes, I set up incubations between the freshwater single-strain CB Candidatus Electronema aureus GS and viruses. The main objective was determining CB abundance during one-month incubation and searching for genomic links to viruses. In addition, several CB genomes were studied bioinformatically to identify defense systems, particularly CRISPR-Cas. One notable result was the unusually high number of spacer sequences on a single CRISPR- Cas array in the Ca. Electronema aureus GS genome. On the other hand, the incubation experiment yielded interesting information, although only partially conclusive. However, an active temperate phage candidate was identified in Ca. Electronema aureus GS genome. Integration of the genome of this temperate phage could have a profound impact on the ecology of this CB, endowing it with protective and novel features, but could eventually have detrimental consequences.
This thesis work brought me to dive into the diversity and structure of bacterial communities in sediments, paying particular attention to those large filamentous bacteria, generally multicellular, that participate in those communities, to finally focus on a little-studied aspect, which is the relationship of those large bacteria with viruses.
Antal sider138
StatusAfsendt - 30 apr. 2023

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