Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean

Abstract

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal-microbial relationships were historically explored in single host-symbiont systems. However, new explorations into the diversity of microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more multi-member microbiome. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment. This review explores the nature of marine animal-microbiome relationships and interactions, and possible factors that may shift associations from symbiotic to dissociated states. I present a brief review of current microbiome research and opportunities, using examples of select marine animals that span diverse phyla within the Animalia, including systems that are more and less developed for symbiosis research, including two represented in my own research program. Lastly, I consider challenges and emerging solutions for moving these and other study systems into a more detailed understanding of host-microbiome interactions within a changing ocean.

The Use of Bioinformatic Tools in Symbiosis and Co-Evolution Studies

“…These processes of co-evolution have been documented by several studies carried out in the organization and composition of host microorganisms (microbiome) in different species [1][2][3][4]. The microbiome is currently considered a functional organ which is fundamental for the host organism, given that studies have shown that this organ is highly dynamic and adaptable, likewise plays an important role in physiological adaptation processes, metabolism, and development [1,2,[4][5][6]. The study of the role of the microbiome for years was limited to those organisms that could be susceptible to culture, the use of techniques based on molecular information (AFLP and RFLP) and denaturing gradient gel electrophoresis (DGGE) could reveal the presence of some species not cultured, but the gel resolution was being the main limitation since a single band could contain more than one sequence [7].…”

“…Higher multicellular organisms have coexisted and co-evolved with resident microorganisms in a relatively harmonious relationship over millions of years, forming a complex organism called holobiont. These processes of co-evolution have been documented by several studies carried out in the organization and composition of host microorganisms (microbiome) in different species [1][2][3][4]. The microbiome is currently considered a functional organ which is fundamental for the host organism, given that studies have shown that this organ is highly dynamic and adaptable, likewise plays an important role in physiological adaptation processes, metabolism, and development [1,2,[4][5][6].…”

“…The development of genomic tools such as the new generation sequencing platforms (NGS) has allowed a better resolution of the diversity present in a given sample through what is known as metagenomics [2,[7][8][9][10]. These same sequencing platforms have allowed not only observing the diversity of a host or environment, but also the functional role of microorganisms as well as their possible interactions with physiological processes or biogeochemical cycles through metatranscriptomics [1,2,4,9]. The understanding of the composition of microorganisms, functions, interactions, and other biological processes through NGS has been done through the development of different bioinformatics tools, which make use of large amounts of information and are able to compare them through different data bases [3,9,11].…”

Liquid biopsies for omics-based analysis in sentinel mussels

“…With the help of recent advances in next generation sequencing, microbiome-associated biomarkers, just like ccfDNA, can be used in clinical practice for risk prediction, diagnosis and progression of a disease, or to predict and modulate response to treatment [13,14]. In marine ecology, microbial biomarkers are also being used for measuring the impact of anthropogenic activities on marine ecosystems [15,16]. In the present work, we have combined the concept of liquid biopsy and the use of FTA cards to develop a liquid biopsy-based sampling method that involves fixation of nucleic acids on FTA cards.…”

Bacteria associated with jellyfish during bloom and post-bloom periods

“…Surfaces of marine animals were found to be a unique habitat for colonization by microorganisms, and the microbial communities associated with living surfaces showed a pronounced variety [1]. Till recently, studies focused on the colonization of benthic organisms such as sponges [2–6], bryozoans [7], and cnidarians, within which are included mainly corals [8–13].…”