Metabolic overlap in environmentally diverse microbial communities

Contains fulltext : 209073.pdf (preprint version ) (Open Access)The majority of microbial communities consist of hundreds to thousands of species, creating a massive network of organisms competing for available resources within an ecosystem. In natural microbial communities it appears that many microbial species have highly redundant metabolisms and seemingly are capable of utilizing the same substrates. This is paradoxical, as theory indicates that species requiring a common resource should outcompete one another. To better understand why microbial species can co-exist, we developed Metabolic Overlap (MO) as a new metric to survey the functional redundancy of microbial communities at the genome scale across a wide variety of ecosystems. Using metagenome-assembled genomes, we surveyed over 1200 studies across ten ecosystem types. We found the highest MO in extreme (i.e., low pH/high temperature) and aquatic environments, while the lowest MO was observed in communities associated with animal hosts, or the built/engineered environment. In addition, different metabolism subcategories were explored for their degree of metabolic overlap. For instance, overlap in nitrogen metabolism was among the lowest in Animal and Engineered ecosystems, while the most was in species from the Built environment. Together, we present a metric that utilizes whole genome information to explore overlapping niches of microbes. This provides a detailed picture of potential metabolic competition and cooperation between species present in an ecosystem, indicates the main substrate types sustaining the community and serves as a valuable tool to generate hypotheses for future research.01 januari 201

Metabolic versatility of the nitrite-oxidizing bacterium Nitrospira marina and its proteomic response to oxygen-limited conditions

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bayer, B., Saito, M. A., McIlvin, M. R., Lucker, S., Moran, D. M., Lankiewicz, T. S., Dupont, C. L., & Santoro, A. E. (2020). Metabolic versatility of the nitrite-oxidizing bacterium Nitrospira marina and its proteomic response to oxygen-limited conditions. Isme Journal, doi:10.1038/s41396-020-00828-3.The genus Nitrospira is the most widespread group of nitrite-oxidizing bacteria and thrives in diverse natural and engineered ecosystems. Nitrospira marina Nb-295T was isolated from the ocean over 30 years ago; however, its genome has not yet been analyzed. Here, we investigated the metabolic potential of N. marina based on its complete genome sequence and performed physiological experiments to test genome-derived hypotheses. Our data confirm that N. marina benefits from additions of undefined organic carbon substrates, has adaptations to resist oxidative, osmotic, and UV light-induced stress and low dissolved pCO2, and requires exogenous vitamin B12. In addition, N. marina is able to grow chemoorganotrophically on formate, and is thus not an obligate chemolithoautotroph. We further investigated the proteomic response of N. marina to low (∼5.6 µM) O2 concentrations. The abundance of a potentially more efficient CO2-fixing pyruvate:ferredoxin oxidoreductase (POR) complex and a high-affinity cbb3-type terminal oxidase increased under O2 limitation, suggesting a role in sustaining nitrite oxidation-driven autotrophy. This putatively more O2-sensitive POR complex might be protected from oxidative damage by Cu/Zn-binding superoxide dismutase, which also increased in abundance under low O2 conditions. Furthermore, the upregulation of proteins involved in alternative energy metabolisms, including Group 3b [NiFe] hydrogenase and formate dehydrogenase, indicate a high metabolic versatility to survive conditions unfavorable for aerobic nitrite oxidation. In summary, the genome and proteome of the first marine Nitrospira isolate identifies adaptations to life in the oxic ocean and provides insights into the metabolic diversity and niche differentiation of NOB in marine environments.We thank John B. Waterbury and Frederica Valois for providing the culture of Nitrospira marina Nb-295T and for continued advice about cultivation. The N. marina genome was sequenced as part of US Department of Energy Joint Genome Institute Community Sequencing Project 1337 to CLD, AES, and MAS in collaboration with the user community. We thank Claus Pelikan for bioinformatic assistance. This research was supported by a Simons Foundation Early Career Investigator in Marine Microbiology and Evolution Award (345889) and US National Science Foundation (NSF) award OCE-1924512 to AES. Proteomics analysis was supported by NSF awards OCE-1924554 and OCE-1850719, and NIH award R01GM135709 to MAS. BB was supported by the Austrian Science Fund (FWF) Project Number: J4426-B (“The influence of nitrifiers on the oceanic carbon cycle”), SL by the Netherlands Organization for Scientific Research (NWO) grant 016.Vidi.189.050, and CLD by NSF award OCE-125999

Diversity patterns and community structure of the ground-associated macrofauna along the beach-inland transition zone of small tropical islands

Biodiversity follows distinct and observable patterns. Where two systems meet, biodiversity is often increased, due to overlapping occurrence ranges and the presence of specialized species that can tolerate the dynamic conditions of the transition zone. One of the most pronounced transition zones occurs at shores, where oceans and terrestrial habitat collide, forming the shore–inland transition zone. The relevance of this transition zone in shaping a system’s community structure is particularly pronounced on small islands due to their high shore-to-inland-area ratio. However, the community structure of insular faunas along this transition zone is unknown. Here, we investigated the diversity patterns along the beach–inland transition zone of small islands and tested the hypothesis that species diversity increases toward the transition zone where beach and interior habitat meet. By measuring environmental parameters, resource availability, and ground-associated macrofauna diversity along transects running across the beach–inland transition zone, we show that a gradual change in species composition from beach to the inland exists, but neither taxa richness, diversity, nor overall abundance changed significantly. These findings offer important insights into insular community structure at the transition zone from sea to land that are relevant to better understand the dynamic and unique characteristics of insular ecosystems

Proteogenomic analysis of Georgfuchsia toluolica revealed unexpected concurrent aerobic and anaerobic toluene degradation

Denitrifying Betaproteobacteria play a key role in the anaerobic degradation of monoaromatic hydrocarbons. We performed a multi-omics study to better understand the metabolism of the representative organism Georgfuchsia toluolica strain G5G6 known as a strict anaerobe coupling toluene oxidation with dissimilatory nitrate and Fe(III) reduction. Despite the genomic potential for degradation of different carbon sources, we did not find sugar or organic acid transporters, in line with the inability of strain G5G6 to use these substrates. Using a proteomics analysis, we detected proteins of fumarate-dependent toluene activation, membrane-bound nitrate reductase, and key components of the metal-reducing (Mtr) pathway under both nitrate- and Fe(III)-reducing conditions. High abundance of the multiheme cytochrome MtrC implied that a porincytochrome complex was used for respiratory Fe(III) reduction. Remarkably, strain G5G6 contains a full set of genes for aerobic toluene degradation, and we detected enzymes of aerobic toluene degradation under both nitrate- and Fe(III)-reducing conditions. We further detected an ATP-dependent benzoyl-CoA reductase, reactive oxygen species detoxification proteins, and cytochrome c oxidase indicating a facultative anaerobic lifestyle of strain G5G6. Correspondingly, we found diffusion through the septa a substantial source of oxygen in the cultures enabling concurrent aerobic and anaerobic toluene degradation by strain G5G6.This work was supported by Wageningen University & Research through its investment theme Resilience, the Technology Foundation (STW), the Applied Science Division of the Dutch Research Council (NWO; project 08053), NWO grant 016.Vidi.189.050, and a Gravitation grant of the Netherlands Ministry of Education, Culture and Science and NWO (project 024.002.002 SIAM). B.K. was supported by the Villum foundation, Denmark (VYI Grant 25491).info:eu-repo/semantics/publishedVersio

Methylotetracoccus oryzae Strain C50C1 Is a Novel Type Ib Gammaproteobacterial Methanotroph Adapted to Freshwater Environments

Methane-oxidizing microorganisms perform an important role in reducing emissions of the greenhouse gas methane to the atmosphere. To date, known bacterial methanotrophs belong to the Proteobacteria, Verrucomicrobia, and NC10 phyla. Within the Proteobacteria phylum, they can be divided into type Ia, type Ib, and type II methanotrophs. Type Ia and type II are well represented by isolates. Contrastingly, the vast majority of type Ib methanotrophs have not been able to be cultivated so far. Here, we compared the distributions of type Ib lineages in different environments. Whereas the cultivated type Ib methanotrophs (Methylococcus and Methylocaldum) are found in landfill and upland soils, lineages that are not represented by isolates are mostly dominant in freshwater environments, such as paddy fields and lake sediments. Thus, we observed a clear niche differentiation within type Ib methanotrophs. Our subsequent isolation attempts resulted in obtaining a pure culture of a novel type Ib methanotroph, tentatively named “Methylotetracoccus oryzae” C50C1. Strain C50C1 was further characterized to be an obligate methanotroph, containing C_(16:1)ω9c as the major membrane phospholipid fatty acid, which has not been found in other methanotrophs. Genome analysis of strain C50C1 showed the presence of two pmoCAB operon copies and XoxF5-type methanol dehydrogenase in addition to MxaFI. The genome also contained genes involved in nitrogen and sulfur cycling, but it remains to be demonstrated if and how these help this type Ib methanotroph to adapt to fluctuating environmental conditions in freshwater ecosystems

Influence of filter age on Fe, Mn and NH4+ removal in dual media rapid sand filters used for drinking water production

Rapid sand filtration is a common method for removal of iron (Fe), manganese (Mn) and ammonium (NH4+) from anoxic groundwaters used for drinking water production. In this study, we combine geochemical and microbiological data to assess how filter age influences Fe, Mn and NH4+ removal in dual media filters, consisting of anthracite overlying quartz sand, that have been in operation for between ∼2 months and ∼11 years. We show that the depth where dissolved Fe and Mn removal occurs is reflected in the filter medium coatings, with ferrihydrite forming in the anthracite in the top of the filters ( 1 m). Removal of NH4+ occurs through nitrification in both the anthracite and sand and is the key driver of oxygen loss. Removal of Fe is independent of filter age and is always efficient (> 97% removal). In contrast, for Mn, the removal efficiency varies with filter age, ranging from 9 to 28% at ∼2–3 months after filter replacement to 100% after 8 months. After 11 years, removal reduces to 60–80%. The lack of Mn removal in the youngest filters (at 2–3 months) is likely the result of a relatively low abundance of mineral coatings that adsorb Mn2+ and provide surfaces for the establishment of a microbial community. 16S rRNA gene amplicon sequencing shows that Gallionella, which are known Fe2+ oxidizers, are present after 2 months, yet Fe2+ removal is mostly chemical. Efficient NH4+ removal (> 90%) establishes within 3 months of operation but leakage occurs upon high NH4+loading (> 160 µM). Two-step nitrification by Nitrosomonas and Candidatus Nitrotoga is likely the most important NH4+ removal mechanism in younger filters during ripening (2 months), after which complete ammonia oxidation by Nitrospira and canonical two-step nitrification occur simultaneously in older filters. Our results highlight the strong effect of filter age on especially Mn2+but also NH4+ removal. We show that ageing of filter medium leads to the development of thick coatings, which we hypothesize leads to preferential flow, and breakthrough of Mn2+. Use of age-specific flow rates may increase the contact time with the filter medium in older filters and improve Mn2+ and NH4+ removal

Cyclic Conversions in the Nitrogen Cycle

The cyclic nature of specific conversions in the nitrogen cycle imposes strict limitations to the conversions observed in nature and explains for example why anaerobic ammonium oxidation (anammox) bacteria can only use nitrite – and not nitrate – as electron acceptor in catabolism, and why nitrite is required as additional electron donor for inorganic carbon fixation in anabolism. Furthermore, the biochemistry involved in nitrite-dependent anaerobic methane oxidation excludes the feasibility of using nitrate as electron acceptor. Based on the cyclic nature of these nitrogen conversions, we propose two scenarios that may explain the ecological role of recently discovered complete ammonia-oxidizing (comammox) Nitrospira spp., some of which were initially found in a strongly oxygen limited environment: (i) comammox Nitrospira spp. may actually catalyze an anammox-like metabolism using a biochemistry similar to intra-oxic nitrite-dependent methane oxidation, or (ii) scavenge all available oxygen for ammonia activation and use nitrate as terminal electron acceptor. Both scenarios require the presence of the biochemical machinery for ammonia oxidation to nitrate, potentially explaining a specific ecological niche for the occurrence of comammox bacteria in nature.BT/Environmental Biotechnolog

Some like it cold : the cellular organization and physiological limits of cold-tolerant nitrite-oxidizing Nitrotoga

Chemolithoautotrophic production of nitrate is accomplished by the polyphyletic functional group of nitrite-oxidizing bacteria (NOB). A widely distributed and important NOB clade in nitrogen removal processes at low temperatures is Nitrotoga, which however remains understudied due to the scarcity of cultivated representatives. Here, we present physiological, ultrastructural and genomic features of Nitrotoga strains from various habitats, including the first marine species enriched from an aquaculture system. Immunocytochemical analyses localized the nitrite-oxidizing enzyme machinery in the wide irregularly shaped periplasm, apparently without contact to the cytoplasmic membrane, confirming previous genomic data suggesting a soluble nature. Interestingly, in two strains we also observed multicellular complexes with a shared periplasmic space, which seem to form through incomplete cell division and might enhance fitness or survival. Physiological tests revealed differing tolerance limits towards dissolved inorganic nitrogen concentrations and confirmed the generally psychrotolerant nature of the genus. Moreover, comparative analysis of 15 Nitrotoga genomes showed, e.g. a unique gene repertoire of the marine strain that could be advantageous in its natural habitat and confirmed the lack of genes for assimilatory nitrite reduction in a strain found to require ammonium for growth. Overall, these novel insights largely broaden our knowledge of Nitrotoga and elucidate the metabolic variability, physiological limits and thus potential ecological roles of this group of nitrite oxidizers