Moving forward with the primate microbiome: Introduction to a special issue of the American Journal of Primatology

Primate microbiome research is a quickly growing field with exciting potential for informing our understanding of primate biology, ecology, and evolution as well as host‐microbe interactions more broadly. This introductory essay to a special section of the American Journal of Primatology provides a cross‐sectional snapshot of current activity in these areas by briefly summarizing the diversity of contributed papers and their relationships to key themes in host‐associated microbiome research. It then uses this survey as a foundation for consolidating a set of key research questions to broadly guide future research. It also argues for the importance of methods standardization to facilitate comparative analyses and the identification of generalizable patterns and relationships. While primatology will benefit greatly from the integration of microbial datasets, it is uniquely positioned to address important questions regarding microbiology and macro‐ecology and evolution more generally. We are eager to see where the primate microbiome leads us.     

Location and distribution of symbiotic bacteria during floral development in Ardisia crispa

Abstract. The location and distribution of symbiotic bacteria during floral development in Ardisia crispa (Thunb.) A.DC., a species characterized by bacterial leaf nodules, has been studied using light, scanning and transmission electron microscopy. During early floral development, bacteria in mucilage derived from host plant trichomes, become enclosed in a small conical chamber on top of the placenta, as a result of the closure and fusion of the carpel initials. The placental epidermal cells, which appear to be secretory in nature, become detached apically in places forming a network of grooves which traverse the placental surface. The symbiotic bacteria are preferentially located in these grooves. As growth and development of the placenta proceed, the grooves widen and deepen to form channels. The cells lining these channels secrete a mucilaginous material. The network of channels covers the entire placental surface and terminates at the placental margins surrounding the ovules. Bacteria are found within the channels, at the ends of the channels near the margin of the placenta, on the surface of the ovules and in the micropyle. It is suggested that these mucilage-filled channels are responsible for, and a prerequisite of, ensuring that the bacterial partner is efficiently transmitted from one host generation to the next by providing a mechanism by which the bacteria arc accurately placed within the developing seed.     

Acetonema longum gen.nov.sp.nov., an H2/CO2 acetogenic bacterium from the termite,Pterotermes occidentis

A previously undescribed, H₂-oxidizing CO₂-reducing acetogenic bacterium was isolated from gut contents of the wood-feeding termite, Pterotermes occidentis. Cells of representative strain APO-1 were strictly anaerobic, Gram-negative, endospore-forming motile rods which measured 0.30–0.40×6–60 m. Cells were catalase positive, oxidase negative, and had 51.5 mol percent G+C in their DNA. Optimum conditions for growth on H₂+CO₂ were at 30–33°C and pH (initial) 7.8, and under these conditions cells formed acetate according to the equation: 4 H₂+2 CO₂CH₃COOH+2 H₂O. Other energy sources supporting good growth of strain APO-1 included glucose, ribose, and various organic acids. Acetate and butyrate were major fermentation products from most organic compounds tested, however propionate, succinate, and 1,2-propanediol were also formed from some substrates. Based on comparative analysis of 16S rRNA nucleotide sequences, strain APO-1 was related to, but distinct from, members of the genus Sporomusa. Moreover, physiological and morphological differences between strain APO-1 and the six known species of Sporomusa were significant. Consequently, it is proposed herewith that a new genus, Acetonema, be established with strain APO-1 as the type strain of the new species, Acetonema longum. A. longum may contribute to the nutrition of P. occidentis by forming acetate, propionate and butyrate, compounds which are important carbon and energy sources for termites.     

Clostridium mayombei sp. nov., an H2/CO2 acetogenic bacterium from the gut of the African soil-feeding termite,Cubitermes speciosus

Clostridium mayombei sp. nov., a previously undescribed H₂-oxidizing CO₂-reducing acetogenic bacterium, was isolated from gut contents of the African soilfeeding termite, Cubitermes speciosus. Cells were anaerobic, Gram positive, catalase and oxidase negative, endospore-forming motile rods which measured 1×2 – 6 m and which had a DNA base composition of 25.6 mol% G+C (strain SFC-5). Optimum conditions for growth on H₂+CO₂ were at 33°C and pH 7.3, and under these conditions cells produced acetate according to the equation: 4 H₂+2 CO₂CH₃COOH+2 H₂O. Other substrates supporting good growth included carbohydrates (e.g. glucose, xylose, starch), sugar alcohols, and organic and amino acids, and with these substrates acetate was almost always the principle fermentation product. Comparative analysis of 16S rRNA nucleotide sequences confirmed that C. mayombei was closely related to various members of the genus Clostridium. However, morphological and physiological differences between C. mayombei and other homoacetogenic clostridia were deemed significant enough to warrant creation of a new taxon. Results are discussed in light of the diversity of H₂/CO₂ acetogens recently isolated from various termites, and in terms of the relative importance of H₂/CO₂ acetogenesis to termite nutrition.     

Emerging roles of low-molecular-weight thiols at the host–microbe interface

Low-molecular-weight (LMW) thiols are an abundant class of cysteine-derived small molecules found in all forms of life that maintain reducing conditions within cells. While their contributions to cellular redox homeostasis are well established, LMW thiols can also mediate other aspects of cellular physiology, including intercellular interactions between microbial and host cells. Here we discuss emerging roles for these redox-active metabolites at the host–microbe interface. We begin by providing an overview of chemical and computational approaches to LMW-thiol discovery. Next, we highlight mechanisms of virulence regulation by LMW thiols in infected cells. Finally, we describe how microbial metabolism of these compounds may influence host physiology.     

Early host–microbe interaction in a peri‐implant oral mucosa‐biofilm model

The host‐microbe relationship is pivotal for oral health as well as for peri‐implant diseases. Peri‐implant mucosa and commensal biofilm play important roles in the maintenance of host‐microbe homeostasis, but little is known about how they interact. We have therefore investigated the early host‐microbe interaction between commensal multispecies biofilm (Streptococcus oralis, Actinomyces naeslundii, Veillonella dispar, Porphyromonas gingivalis) and organotypic peri‐implant mucosa using our three‐dimensional model. After 24 hr, biofilms induced weak inflammatory reaction in the peri‐implant mucosa by upregulation of five genes related to immune response and increased secretion of IL‐6 and CCL20. Biofilm volume was reduced which might be explained by secretion of β‐Defensins‐1, ‐2, and CCL20. The specific tissue reaction without intrinsic overreaction might contribute to intact mucosa. Thus, a relationship similar to homeostasis and oral health was established within the first 24 hr. In contrast, the mucosa was damaged and the bacterial distribution was altered after 48 hr. These were accompanied by an enhanced immune response with upregulation of additional inflammatory‐related genes and increased cytokine secretion. Thus, the homeostasis‐like relationship was disrupted. Such profound knowledge of the host‐microbe interaction at the peri‐implant site may provide the basis to improve strategies for prevention and therapy of peri‐implant diseases.     

Do soil inoculants accelerate dryland restoration? A simultaneous assessment of biocrusts and mycorrhizal fungi

Biological soil crusts (biocrusts) and arbuscular mycorrhizal (AM) fungi are communities of soil organisms often targeted to assist in the achievement of multiple ecological restoration goals. In drylands, benefits conferred from biocrust and AM fungal inoculation, such as improved native plant establishment and soil stabilization, have primarily been studied separately. However, comparisons between these two types of soil inoculants and investigations into potential synergies between them, particularly at the plant community scale, are needed to inform on‐the‐ground management practices in drylands. We conducted two full‐factorial experiments—one in greenhouse mesocosms and one in field plots—to test the effects of AM fungal inoculation, biocrust inoculation, and their interaction on multiple measures of dryland restoration success. Biocrust inoculation promoted soil stabilization and plant drought tolerance, but had mixed effects on native plant diversity (positive in greenhouse, neutral in field) and productivity (negative in greenhouse, neutral in field). In greenhouse mesocosms, biocrust inoculation reduced plant biomass, which was antagonistic to % root length colonized by AM fungi. Inoculation with native or commercial AM fungi did not influence plant establishment, drought tolerance, or soil stabilization in either study, and few synergistic effects of simultaneous inoculation of AM fungi and biocrusts were observed. These results suggest that, depending on the condition of existing soil communities, inoculation with AM fungi may not be necessary to promote dryland restoration goals, while inoculation with salvaged biocrust inoculation may be beneficial in some contexts.     

Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds

The gut microbiome of animals, which serves important functions but can also contain potential pathogens, is to varying degrees under host genetic control. This can generate signals of phylosymbiosis, whereby gut microbiome composition matches host phylogenetic structure. However, the genetic mechanisms that generate phylosymbiosis and the scale at which they act remain unclear. Two non‐mutually exclusive hypotheses are that phylosymbiosis is driven by immunogenetic regions such as the major histocompatibility complex (MHC) controlling microbial composition, or by spatial structuring of neutral host genetic diversity via founder effects, genetic drift, or isolation by distance. Alternatively, associations between microbes and host phylogeny may be generated by their spatial autocorrelation across landscapes, rather than the direct effects of host genetics. In this study, we collected MHC, microsatellite, and gut microbiome data from separate individuals belonging to the Galápagos mockingbird species complex, which consists of four allopatrically distributed species. We applied multiple regression with distance matrices and Bayesian inference to test for correlations between average genetic and microbiome similarity across nine islands for which all three levels of data were available. Clustering of individuals by species was strongest when measured with microsatellite markers and weakest for gut microbiome distributions, with intermediate clustering of MHC allele frequencies. We found that while correlations between island‐averaged gut microbiome composition and both microsatellite and MHC dissimilarity existed across species, these relationships were greatly weakened when accounting for geographic distance. Overall, our study finds little support for large‐scale control of gut microbiome composition by neutral or adaptive genetic regions across closely related bird phylogenies, although this does not preclude the possibility that host genetics shapes gut microbiome at the individual level.     

Gastrointestinal stress as innate defence against microbial attack

The human gastrointestinal (GI) tract has been bestowed with the most difficult task of protecting the underlying biological compartments from the resident commensal flora and the potential pathogens in transit through the GI tract. It has a unique environment in which several defence tactics are at play while maintaining homeostasis and health. The GI tract shows myriad number of environmental extremes, which includes pH variations, anaerobic conditions, nutrient limitations, elevated osmolarity etc., which puts a check to colonization and growth of nonfriendly microbial strains. The GI tract acts as a highly selective barrier/platform for ingested food and is the primary playground for balance between the resident and uninvited organisms. This review focuses on antimicrobial defense mechanisms of different sections of human GI tract. In addition, the protective mechanisms used by microbes to combat the human GI defence systems are also discussed. The ability to survive this innate defence mechanism determines the capability of probiotic or pathogen strains to confer health benefits or induce clinical events respectively.