Mammalian microbiomes

Endothermic (an organism that maintains its body at a metabolically favourable temperature) amniotes (who lay their eggs on land or retain the fertilised egg within the mother), also known as mammals, count among their cohort the largest (whales) and the most intelligent (some primates, cetaceans and elephants) animals on Earth. However, none of the 5488 mammalian species live alone since they all support a complex menagerie of microbes including prokaryotes (Bacteria and Archaea), microbial eukaryotes, and viruses. That so-called ‘microbiome’ plays myriad roles ranging from the very well known and well studied (disease) through to provocative involvements (mood alteration and brain activity). Indeed even the microbiome has been subdivided by some into the bacteriome, the mycobiome and the virome. It is very timely that this issue be devoted to mammalian microbiomes since the study of microbiomes is going through an unprecedented revolution due to current and projected capabilities to generate metagenome sequences, determine metatranscriptomic, metaproteomic and metametabolomic information and crucially, analyse the deluge of data and interpret findings ecologically. The novel procedures are broadly in the economic realm of numerous researchers, but many do pose considerable technical challenges. The practical outcomes for host species and their environments are diverse.

Fundamental and applied host microbiome research began very early in the history of microbiology. Indeed, Antonie van Leeuwenhoek (1632–1723), ‘the father of microbiology’, observed and reported on what were large selenomonads from the human mouth in 1676. More recently, Robert Hungate¹ (1906–2004), ‘the father of rumen microbiology’, developed critical techniques that allowed the study of anaerobic microbes – the roll tube technique². Using this method that he meticulously described, he explored methanogenesis and cellulose biochemistry (among other metabolic functions) in ruminants and the microbial ecology of monkey and human guts. The practical outcomes of improved milk, meat and wool production were major drivers to rumen microbiology studies.

It has been nearly four decades since ‘Sanger DNA sequencing’ was introduced³, the first organism was sequenced⁴ and ribosomal RNA analysis was used to determine the third domain of cellular life on Earth, the Archaea⁵. Since the late 1970s, substantial method developments including polymerase chain reaction (PCR), improved acquisition of DNA sequences (automated DNA sequencing) and their analyses have occurred. The first decade of this century was part of that method improvement and subsequent data eruption. These fundamental discoveries in the late 1970s were paramount in facilitating mammalian microbiome research.

The diversity of prokaryotes in a plethora of environments could be comprehended by applying massively parallel high throughput DNA sequencing methods (starting with 454 Life Sciences ‘pyrosequencing’ in 2005) to small subunit rRNA genes. Full genomes were determined in large numbers (currently of 31,241 prokaryotes), whole-genome phylogenies were reported, and the ‘meta-omics’ fields of endeavour were well and truly spawned into the general arena of the Microbiome. The giddy rate of progress in omics is difficult to keep pace with but critical questions about microbial function and dynamics (stable and mobile) and the chemical interplay between microbes and their hosts should be overriding drivers of their investigation, particularly in mammals. Pondering the future of microbiome research, a collection of authors recently reported on their individual opinions⁶, and to quote from this paper:

Overall, future microbiome research regarding the molecules and mechanisms mediating interactions between members of microbial communities and their hosts should lead to discovery of exciting new biology and transformative therapeutics.

The articles in this Microbiology Australia issue cover a broad range of mammalian microbiome studies in Australia. The majority are on humans (oral and gut), but marine mammals (skin, gut and respiratory tract including blowhole), ruminants and terrestrial Australian native animals (oral and gut) are also explored. The motivations for the host-microbe studies in these papers cover the host species from both health and well-being perspectives as well as from general ecological and animal production improvement viewpoints. Monotreme microbial ecology and potential biotechnological discoveries from the consumption of toxic diets (e.g. those high in essential oils like Eucalyptus spp.) should attract more attention and are of essential Australian relevance.