Integrative and Comparative Biology Integrative and Comparative Biology, Volume 60, Number 2, Pp
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Integrative and Comparative Biology Integrative and Comparative Biology, volume 60, number 2, pp. 288–303 doi:10.1093/icb/icaa022 Society for Integrative and Comparative Biology SYMPOSIUM Phenotypic Comparability from Genotypic Variability among Physically Structured Microbial Consortia Downloaded from https://academic.oup.com/icb/article/60/2/288/5827464 by College of Charleston user on 02 October 2020 Stephanie K. Hoffman ,1,*,† Kiley W. Seitz,*,‡ Justin C. Havird ,*,§ David A. Weese,*,¶ and Scott R. Santos* *Department of Biological Sciences and Molette Laboratory for Climate Change and Environmental Studies, Auburn University, Auburn, AL 36849, USA; †Department of Biological Sciences, Green River College, Auburn, WA 98092, USA; ‡Strutural and Computational Biology Unit, European Molecular Biological Laboratory, 69117 Heidelberg, Germany; §Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712, USA; ¶Department of Biological and Environmental Sciences, Georgia College & State University, Milledgeville, GA 31061, USA From the symposium “SICB Wide Symposium: Building Bridges from Genome to Phenome: Molecules, Methods and Models” presented at the annual meeting of the Society for Integrative and Comparative Biology January 3–7, 2020 at Austin, Texas. 1E-mail: [email protected] Synopsis Microbiomes represent the collective bacteria, archaea, protist, fungi, and virus communities living in or on individual organisms that are typically multicellular eukaryotes. Such consortia have become recognized as having significant impacts on the development, health, and disease status of their hosts. Since understanding the mechanistic connections between an individual’s genetic makeup and their complete set of traits (i.e., genome to phenome) requires consideration at different levels of biological organization, this should include interactions with, and the organization of, microbial consortia. To understand microbial consortia organization, we elucidated the genetic constituents among phenotypically similar (and hypothesized functionally-analogous) layers (i.e., top orange, second orange, pink, and green layers) in the unique laminated orange cyanobacterial–bacterial crusts endemic to Hawaii’s anchialine ecosystem. High- throughput amplicon sequencing of ribosomal RNA hypervariable regions (i.e., Bacteria-specific V6 and Eukarya-biased V9) revealed microbial richness increasing by crust layer depth, with samples of a given layer more similar to different layers from the same geographic site than to their phenotypically-analogous layer from different sites. Furthermore, samples from sites on the same island were more similar to each other, regardless of which layer they originated from, than to analogous layers from another island. However, cyanobacterial and algal taxa were abundant in all surface and bottom layers, with anaerobic and chemoautotrophic taxa concentrated in the middle two layers, suggesting crust oxygenation from both above and below. Thus, the arrangement of oxygenated vs. anoxygenated niches in these orange crusts is functionally distinct relative to other laminated cyanobacterial–bacterial communities examined to date, with convergent evolution due to similar environmental conditions a likely driver for these phenotypically comparable but genetically distinct microbial consortia. Introduction Biology (SICB), much work remains toward under- Elucidating relationships between the genetic make- standing the mechanistic basis of the “genome to up(i.e., genome) of an individual and its entirety of phenome” in spite of numerous technological advan- potential physical and/or physiological characteristics ces in this area. Among these challenges is the need or traits (i.e., phenome) are among the Grand to encompass different levels of biological organiza- Challenges currently confronting biologists. As evi- tion, and recognize that important phenotypes such dent from the “Building Bridges from Genome to as development, health, and disease status can be Phenome” symposium at the 2020 Annual Meeting attributed to the identity and genetics of microor- of the Society for Integrative and Comparative ganisms intimately associated with the specific Advance Access publication April 30, 2020 ß The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. Consortia phenotype comparability 289 individual in both plants (e.g., Beilsmith et al. 2019) salinities originating from subsurface connections and animals (e.g., Dube et al. 2019), including (or influences) from fresh groundwater and seawater humans (e.g., Valles-Colomer et al. 2019; Zeevi ( Holthuis 1973; Maciolek 1983; Stock et al. 1986; et al. 2019). Such consortia, representing the collec- Sket 1996). Habitats fitting this description are lo- tive bacteria, archaea, protist, fungi, and virus com- cated primarily in the tropics (Holthuis 1973; Bishop munities living in or on typically multicellular et al. 2004; Krstulovic et al. 2013; Menning et al. eukaryotes (Whipps et al. 1988; Prescott 2017), 2014) and occur within a variety of basin substrates have become a target of intensive research over the (Holthuis 1973; Maciolek 1983; Sket 1996) where last 15–20 years both for various organisms (reviewed complex physical and chemical clines can occur Downloaded from https://academic.oup.com/icb/article/60/2/288/5827464 by College of Charleston user on 02 October 2020 by Cani 2018) and natural and man-made environ- within the water column (Stock et al. 1986; ments (reviewed by Gilbert and Stephens 2018; Humphreys 1999; Bishop et al. 2004). Although the Jansson and Hofmockel 2020). However, while dis- anchialine ecosystem has been found to host high cussions of “genome to phenome” should be consid- levels of species richness and endemism when it ered incomplete without accounting for microbial comes to macroorganisms (Yager 1981; Brock and consortia interactions and organization, explicit Bailey-Brock 1998; Iliffe 2002; Mejıa-Ortız et al. studies in this context have been largely lacking. 2007), less work has been done on the microbial Given current interests in the impacts of microbial communities within them (Sarbu et al. 1996; consortia on the phenotypes of organisms and the Seymour et al. 2007; Gonzalez et al. 2011; environment, it should not be surprising that intense Humphreys et al. 2012). attention is being paid to further identify and de- Confined to the Cape Kinau and Kona regions of velop models for such research. Efforts focused on Maui and Hawaii, respectively (Wong 1975; Bailey- plants and animals have gravitated to taxa that are Brock and Brock 1993; Hoffman et al. 2018a, 2018b), time-efficient, cost-effective, and rich in tools and the endemic laminated orange microbial crust com- resources (reviewed in Compant et al. 2019; munities from the Hawaiian anchialine ecosystem Douglas 2019). In contrast, the great heterogeneity (Fig. 1) have structures comparable to stromatolites, among and within aquatic and terrestrial environ- laminated mats, or microbialites in being comprised ments makes identifying a specific, and widely appli- of multiple discernable (i.e., top orange, second or- cable, model more difficult. However, particular ange, pink, and green) layers. Each layer is primarily microbial consortia have garnered interest given their composed of filamentous cyanobacteria and multi- unusual or unique phenotype or properties. cellular algae colonized by diatoms and other micro- Laminated microbial mats, in which taxa exhibit ver- organisms based on microscopy studies (Wong 1975; tically stratified distributions in response to environ- Bailey-Brock and Brock 1993). Structurally, stroma- mental and/or chemical gradients, have proven to be tolites and other laminated microbial mats exhibit a a source of valuable biological and technological dis- common phenotype that can be subdivided from the coveries. For example, fossilized mats are central for surface to the base in a manner apparently depen- studying the evolution of life (Walter et al. 1972; dent on physical and environmental properties such Konhauser et al. 2003; Nutman et al. 2016) and as the presence or absence of oxygen and/or light predicting how life may evolve on other planets penetration. These stratifications generally include a (Walker et al. 2005) while extant ones have yielded surface oxic photic zone overlaying anoxic photic organisms with high biotechnological value like and anoxic aphotic zones (Bolhuis et al. 2014) with Thermus aquaticus (Chien et al. 1976; Ishino and distinct taxa occupying each niche, specifically oxy- Ishino 2014). While some laminated microbial genic phototrophs and aerobic heterotrophs most mats from particular ecosystems have received spe- often near the surface while anaerobic phototrophs cial interest or extensive study like those in the such as Chromatiales, Rhodobacterales, and Yellowstone (USA) hot springs (Ferris and Ward Rhodospirillales and sulfate-reducing bacteria like 1997; Ward et al. 2006; Becraft et al. 2011) and the Syntrophobacterales occurring in deeper zones Hamelin Pool (AU) stromatolites (Awramik and (Paerl et al. 2000; Fourc¸ans et al. 2004; Armitage Riding 1988; Papineau et al. 2005; Suosaari et al. et al. 2012; Bolhuis et al. 2014). Although represent- 2016), many others have largely remained underex- ing just 10–20% of the total microbial population plored, including the unique,