title: Phylogenetic patterns in the microbial response to resource availability: amino acid incorporation in San Francisco Bay.
abstract: Aquatic microorganisms are typically identified as either oligotrophic or copiotrophic, representing trophic strategies adapted to low or high nutrient concentrations, respectively. Here, we sought to take steps towards identifying these and additional adaptations to nutrient availability with a quantitative analysis of microbial resource use in mixed communities. We incubated an estuarine microbial community with stable isotope labeled amino acids (AAs) at concentrations spanning three orders of magnitude, followed by taxon-specific quantitation of isotopic incorporation using NanoSIMS analysis of high-density microarrays. The resulting data revealed that trophic response to AA availability falls along a continuum between copiotrophy and oligotrophy, and high and low activity. To illustrate strategies along this continuum more simply, we statistically categorized microbial taxa among three trophic types, based on their incorporation responses to increasing resource concentration. The data indicated that taxa with copiotrophic-like resource use were not necessarily the most active, and taxa with oligotrophic-like resource use were not always the least active. Two of the trophic strategies were not randomly distributed throughout a 16S rDNA phylogeny, suggesting they are under selective pressure in this ecosystem and that a link exists between evolutionary relatedness and substrate affinity. The diversity of strategies to adapt to differences in resource availability highlights the need to expand our understanding of microbial interactions with organic matter in order to better predict microbial responses to a changing environment.
authors.affiliation: Physical and Life Science Directorate, Lawrence Livermore National Laboratory, Livermore California, United States of America.
authors.forename: Xavier
authors.initials: X
authors.lastname: Mayali
authors.affiliation: Physical and Life Science Directorate, Lawrence Livermore National Laboratory, Livermore California, United States of America.
authors.forename: Peter K
authors.initials: PK
authors.lastname: Weber
authors.affiliation: Physical and Life Science Directorate, Lawrence Livermore National Laboratory, Livermore California, United States of America.
authors.forename: Shalini
authors.initials: S
authors.lastname: Mabery
authors.affiliation: Physical and Life Science Directorate, Lawrence Livermore National Laboratory, Livermore California, United States of America.
authors.forename: Jennifer
authors.initials: J
authors.lastname: Pett-Ridge
mesh_terms: D000596:Amino Acids / Q000378:metabolism*; D061006:Bays / Q000382:microbiology*; D004275:DNA, Ribosomal / Q000235:genetics; D017753:Ecosystem; D007553:Isotope Labeling / Q000379:methods; D010802:Phylogeny; D012495:San Francisco
chemical_list: D000596:Amino Acids; D004275:DNA, Ribosomal
references.citation: Microb Ecol. 1997 Jan;33(1):11-20
references.pmid: 9039761
references.citation: ISME J. 2013 May;7(5):896-907
references.pmid: 23235289
references.citation: Environ Microbiol. 2010 Mar;12(3):616-27
references.pmid: 19930445
references.citation: Genome Res. 2009 May;19(5):744-56
references.pmid: 19411599
references.citation: Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15527-33
references.pmid: 19805210
references.citation: Ecol Lett. 2006 Feb;9(2):228-41
references.pmid: 16958887
references.citation: ISME J. 2010 Jun;4(6):784-98
references.pmid: 20072162
references.citation: Nature. 2002 Dec 19-26;420(6917):806-10
references.pmid: 12490947
references.citation: Nat Biotechnol. 1999 Oct;17(10):974-8
references.pmid: 10504697
references.citation: Proc Natl Acad Sci U S A. 2008 Mar 18;105(11):4209-14
references.pmid: 18337491
references.citation: FEMS Microbiol Ecol. 2002 Feb 1;39(2):91-100
references.pmid: 19709188
references.citation: Science. 2012 May 4;336(6081):608-11
references.pmid: 22556258
references.citation: Bioessays. 2001 Jul;23(7):657-61
references.pmid: 11462219
references.citation: Appl Environ Microbiol. 2005 Oct;71(10):5665-77
references.pmid: 16204474
references.citation: Science. 2005 Aug 19;309(5738):1242-5
references.pmid: 16109880
references.citation: Appl Environ Microbiol. 2006 Mar;72(3):2141-7
references.pmid: 16517664
references.citation: Appl Environ Microbiol. 2004 Jul;70(7):4129-35
references.pmid: 15240292
references.citation: Appl Environ Microbiol. 2010 Feb;76(4):1278-81
references.pmid: 20023110
references.citation: Appl Environ Microbiol. 1980 Jun;39(6):1085-95
references.pmid: 16345577
references.citation: ISME J. 2011 May;5(5):856-65
references.pmid: 21068774
references.citation: Ann Rev Mar Sci. 2011;3:567-99
references.pmid: 21329217
references.citation: Appl Environ Microbiol. 2007 Jun;73(11):3528-35
references.pmid: 17400772
references.citation: Arch Microbiol. 2000 Feb;173(2):138-45
references.pmid: 10795685
references.citation: ISME J. 2012 Jun;6(6):1210-21
references.pmid: 22158395
references.citation: Philos Trans R Soc Lond B Biol Sci. 2006 Nov 29;361(1475):2009-21
references.pmid: 17062417
references.citation: Science. 2008 May 23;320(5879):1081-5
references.pmid: 18497299
references.citation: Nature. 2009 Oct 15;461(7266):976-9
references.pmid: 19794413
references.citation: Appl Environ Microbiol. 2000 Nov;66(11):4634-40
references.pmid: 11055904
references.citation: J Bacteriol. 1982 Jan;149(1):1-5
references.pmid: 7054139
references.citation: Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6578-83
references.pmid: 9618454
references.citation: Nature. 2010 Nov 4;468(7320):60-6
references.pmid: 21048761